Phloem-Borne FT Signals Flowering in Cucurbits

Approximately 45 years ago, Zeevaart (1962) wrote that the identification of florigen, a phloem-borne signaling molecule that acts to initiate photoperiodic-dependent flowering, was the most urgent problem in the study of the physiology of flowering and expressed hope that the recent isolation of a flower-inducing extract from Xanthium (Lincoln et al., 1960) would lead to a solution. In the ensuing years, our knowledge of the phenomenon of photoperiodically induced flowering has vastly expanded to include knowledge of the photoreceptors involved and integration with the circadian clock, with other floral induction pathways, and with the downstream genes that control flower morphogenesis in the shoot apex; yet, the nature of florigen has remained a mystery for most of that time. It is only very recently that evidence has begun building for a primary role for FLOWERING LOCUS T (FT), which encodes a RAF kinase inhibitor– like protein, as a key component of the florigenic signal (reviewed in Corbesier and Coupland, 2006; Imaizumi and Kay, 2006). In Arabidopsis, FT and SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), which encodes a MADS box transcription factor, are considered floral integrator genes because together they receive input from the four main flowering time pathways: the photoperiodic, autonomous, vernalization, and gibberellin pathways. FT interacts with the bZIP transcription factor FD, which leads to upregulation of SOC1. This is one of the early signs of the transition to flowering and in turn leads to activation of the floral initiation genes LFY and AP1 in the shoot apical meristem (SAM) (Borner et al., 2000; Samach et al., 2000). FT is expressed in the vascular tissue of plant leaves but not in the SAM (Takada and Goto, 2003; An et al., 2004), and FD is expressed only in the SAM (Abe et al., 2005; Wigge et al., 2005). This implies that FT mRNA, FT protein, or both act as florigenic signals, either alone or together with other unknown components of the signal. FT is a small protein of ;23 kD, which is below the size exclusion limit of plasmodesmata connecting companion cells to the sieve tube system (Imlau et al., 1999), and therefore might move freely through the phloem. An et al. (2004) suggested that the activation of FT in the phloem (by photoperiodic or other signals) might precede movement of the FT protein to the meristem. Huang et al. (2005) then reported that FT mRNA moves from the leaves to shoot apices and induces flowering in Arabidopsis, although this study did not rule out a possible role for transport of FT protein. Contrasting data from grafting experiments in tomato revealed that the FT ortholog expressed in leaves could induce flowering in a distant shoot meristem but that transcripts of the inducing FT gene could not be detected in the meristem (Lifschitz et al., 2006). Corbesier and Coupland (2006) noted that ‘‘whether the FT mRNA, the FT protein or both move in wild-type plants remains to be established, as does the requirement of any movement for flowering.’’ Recently, the article of Huang et al. (2005) was retracted because the primary RT-PCR data regarding FT mRNA movement into the apex was found to be flawed (Böhlenius et al., 2007). At the same time, two new articles appeared, one suggesting that FT protein acts as a non-cell-autonomous signal to induce flowering in Arabidopsis (Corbesier et al., 2007) and the other that its homolog in rice, called Hd3a, has the same activity (Tamaki et al., 2007). In this issue of The Plant Cell, Lin et al. (pages 1488–1506) provide some of the strongest evidence to date that FT protein functions as a long-distance florigenic signal, from work performed in cucurbits (squash). The authors used a Cucurbita moschata accession responsive to inductive short-day (SD) photoperiods, along with a potyvirus vector, Zucchini yellow mosaic virus, to drive FT expression under different daylength growing conditions. They also performed grafting experiments between uninduced C. moschata and flowering Cucurbita maxima, a day-neutral species. Analysis of vascular tissue and phloem sap from photoperiodically induced and uninduced plants by real-time RT-PCR and mass spectrometry showed that the presence in the phloem of FT-like (FTL) proteins, but not FTL mRNA, was highly correlated with the onset of flowering.