The gated induction system of a systemic floral inhibitor, antiflorigen, determines obligate short-day flowering in chrysanthemums

Abstract

Photoperiodic floral induction has had a significant impact on the agricultural and horticultural industries. Changes in day length are perceived in leaves, which synthesize systemic flowering inducers (florigens) and inhibitors (antiflorigens) that determine floral initiation at the shoot apex. Recently, FLOWERING LOCUS T (FT) was found to be a florigen; however, the identity of the corresponding antiflorigen remains to be elucidated. Here, we report the identification of an antiflorigen gene, Anti-florigenic FT/TFL1 family protein (AFT), from a wild chrysanthemum (Chrysanthemum seticuspe) whose expression is mainly induced in leaves under noninductive conditions. Gain-and loss-of-function analyses demonstrated that CsAFT acts systemically to inhibit flowering and plays a predominant role in the obligate photoperiodic response. A transient gene expression assay indicated that CsAFT inhibits flowering by directly antagonizing the flower-inductive activity of CsFTL3, a C. seticuspe ortholog of FT, through interaction with CsFDL1, a basic leucine zipper (bZIP) transcription factor FD homolog of Arabidopsis. Induction of CsAFT was triggered by the coincidence of phytochrome signals with the photosensitive phase set by the dusk signal; flowering occurred only when night length exceeded the photosensitive phase for CsAFT induction. Thus, the gated antiflorigen production system, a phytochrome-mediated response to light, determines obligate photoperiodic flowering response in chrysanthemums, which enables their year-round commercial production by artificial lighting. T he transition from the vegetative to the reproductive phase is one of the most important developmental stages in the plant life cycle. The timing of flowering during the year, which is an important adaptive trait that strongly influences reproductive fitness, is affected by both endogenous and environmental factors. Changes in day length (photoperiod) are among the most important and reliable seasonal signals to plants to reproduce at favorable times of the year. In 1920, Garner and Allard (1) demonstrated that several plant species flower in response to changes in day length and described this phenomenon as "photoperiodism." Plants are classified according to their photoperiodic responses as short-day plants (SDP), in which flowering occurs when the night length is longer than a critical minimum, long-day plants (LDP), in which flowering occurs when the day becomes longer than some crucial length, and day-neutral plants.Within the SDP and LDP, there are obligate (qualitative) and facultative (quantitative) types of photoperiodic responses. Obligate-type plants are those in which a particular photoperiod is an absolute requirement for the occurrence of a response. Chrysanthemum has become one of the most important horticultural crops since the discovery of photoperiodism because the flowering time of this obligate SDP can be strictly controlled by the use of blackouts or artificial lighting, day-length extension, or illumination during the middle of the...

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