Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways

Abstract

A complex consisting of evolutionarily conserved FD, flowering locus T (FT) proteins is a regulator of floral transition. Intriguingly, FT orthologs are also implicated in developmental transitions distinct from flowering, such as photoperiodic control of bulbing in onions, potato tuberization, and growth cessation in trees. However, whether an FT-FD complex participates in these transitions and, if so, its mode of action, are unknown. We identified two closely related FD homologs, FD-like 1 (FDL1) and FD-like 2 (FDL2), in the model tree hybrid aspen. Using gain of function and RNAi-suppressed FDL1 and FDL2 transgenic plants, we show that FDL1 and FDL2 have distinct functions and a complex consisting of FT and FDL1 mediates in photoperiodic control of seasonal growth. The downstream target of the FT-FD complex in photoperiodic control of growth is Like AP1 (LAP1), a tree ortholog of the floral meristem identity gene APETALA1. Intriguingly, FDL1 also participates in the transcriptional control of adaptive response and bud maturation pathways, independent of its interaction with FT, presumably via interaction with abscisic acid insensitive 3 (ABI3) transcription factor, a component of abscisic acid (ABA) signaling. Our data reveal that in contrast to its primary role in flowering, FD has dual roles in the photoperiodic control of seasonal growth and stress tolerance in trees. Thus, the functions of FT and FD have diversified during evolution, and FD homologs have acquired roles that are independent of their interaction with FT.

Keywords: adaptive response; bud set; growth cessation; hybrid aspen; seasonal growth.

Fig. 1.

Bud formation in WT and FDL1oe (lines 3A and 5A) plants. A, D, and G represent plants growing in long days (LD). WT plants had ceased growth and developed buds (B and C), but the FDL1oe plants had not (E and H). (F and I) FDL1oe plants set buds after 10 wk (W) of SDs. Arrows indicate apical buds.

Fig. 2.

Analysis of interaction between hybrid aspen FD and FT homologs. FDL1 interacts with hybrid aspen FT1 and FT2 to activate OsMADS15 expression when coexpressed in rice protoplasts. Plasmid DNA for expressing FT and FD homologs from rice or poplar was transformed into rice protoplasts, and OsMADS15 induction was assayed by quantitative RT-PCR analysis. cDNAs expressed and the OsMADS15/ubiquitin expression ratio 24 h after the transformation are shown on the x and y axes, respectively. Error bars indicate SDs of triplicate measurements.

Fig. 3.

FDL1 mediates in the photoperiodic control of LAP1 expression. Expression of LAP1 in the WT and FDL1oe plants (A) and expression of LAP1 in the WT and FDL1RNAi plants after SDs (B). The duration of SDs is shown (in weeks) on the x axis, and LAP1 expression (relative to the reference gene TIP41-like, average for three biological replicates ± SE) is shown on the y axis.

Fig. 4.

Photoperiodic control of FDL1 expression. SD induction of FDL1 expression is attenuated in FT1oe plants. The duration of SDs is shown (in weeks) on the x axis. Induction of FDL1 expression in SDs (relative to the reference gene TIP41-like, average for three biological replicates ± SE) is plotted relative to expression in long days (0 wk SDs) on the y axis.

Fig. 5.

FDL1 mediates in SD-controlled adaptive response and bud maturation pathways. Expression pattern of markers for adaptive response (LEA and OSM) and bud maturation (CHS and C4H) in FDL1oe (A; line) and FDL1RNAi (B; line) apices are compared with WT plants. Expression of the cited genes is shown relative to the reference gene TIP41-like on the y axis (average for three biological replicates ± SE), and duration of SDs (in weeks) is shown on the x axis.

Fig. 6.

Interaction of FDL1 and ABI3 proteins. c-Myc–FDL1 and HA-tagged ABI3 (HA-ABI3) were coexpressed in Arabidopsis protoplasts derived from cell suspension cultures. c-Myc–FDL1 was immunoprecipitated (IP) from the protein extracts using anti–c-Myc antibody, and HA-ABI3 was then assayed with anti-HA antibody by Western blot (WB). (Lower) c-Myc–FDL1 bound to the beads was revealed using anti–c-Myc antibody.