Long-range mobile signals mediate seasonal control of shoot growth.

In perennial plants, seasonal shifts provide cues that control adaptive growth patterns of the shoot apex. However, where these seasonal cues are sensed and communicated to the shoot apex remains unknown. We demonstrate that systemic signals from leaves play key roles in seasonal control of shoot growth in model tree hybrid aspen. Grafting experiments reveal that the tree ortholog of Arabidopsis flowering time regulator FLOWERING LOCUS T (FT) and the plant hormone gibberellic acid (GA) systemically convey seasonal cues to the shoot apex. GA (unlike FT) also acts locally in shoot apex, downstream of FT in seasonal growth control. At the shoot apex, antagonistic factors-LAP1, a target of FT and the FT antagonist TERMINAL FLOWER 1 (TFL1)-act locally to promote and suppress seasonal growth, respectively. These data reveal seasonal changes perceived in leaves that are communicated to the shoot apex by systemic signals that, in concert with locally acting components, control adaptive growth patterns.

Abscisic acid signalling mediates biomass trade-off and allocation in poplar.

Abscisic acid (ABA) is a well known stress hormone regulating drought adaptation of plants. Here, we hypothesised that genetic engineering of genes involved in ABA stress signalling and photoperiodic regulation affected drought resistance by trade-off with biomass production in perennial poplar trees. We grew Populus tremula × tremuloides wild-type (T89) and various transgenic lines (two transformation events of 35S::abi1-1, 35S::RCAR, RCAR:RNAi, 35S::ABI3, 35S::AREB3, 35S::FDL1, FDL1:RNAi, 35S::FDL2 and FDL2:RNAi) outdoors and exposed them to drought in the second growth period. After the winter, the surviving lines showed a huge variation in stomatal conductance, leaf size, whole-plant leaf area, tree height, stem diameter, and biomass. Whole-plant leaf area was a strong predictor for woody biomass production. The 35S::AREB3 lines were compromised in biomass production under well irrigated conditions compared with wild-type poplars but were resilient to drought. ABA signalling regulated FDL1 and FDL2 expression under stress. Poplar lines overexpressing FDL1 or FDL2 were drought-sensitive; they shed leaves and lost root biomass, whereas the FDL RNAi lines showed higher biomass allocation to roots under drought. These results assign a new function in drought acclimation to FDL genes aside from photoperiodic regulation. Our results imply a critical role for ABA-mediated processes in balancing biomass production and climate adaptation.

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

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.

A genetic network mediating the control of bud break in hybrid aspen.

In boreal and temperate ecosystems, temperature signal regulates the reactivation of growth (bud break) in perennials in the spring. Molecular basis of temperature-mediated control of bud break is poorly understood. Here we identify a genetic network mediating the control of bud break in hybrid aspen. The key components of this network are transcription factor SHORT VEGETATIVE PHASE-LIKE (SVL), closely related to Arabidopsis floral repressor SHORT VEGETATIVE PHASE, and its downstream target TCP18, a tree homolog of a branching regulator in Arabidopsis. SVL and TCP18 are downregulated by low temperature. Genetic evidence demonstrates their role as negative regulators of bud break. SVL mediates bud break by antagonistically acting on gibberellic acid (GA) and abscisic acid (ABA) pathways, which function as positive and negative regulators of bud break, respectively. Thus, our results reveal the mechanistic basis for temperature-cued seasonal control of a key phenological event in perennial plants.

A tree ortholog of APETALA1 mediates photoperiodic control of seasonal growth.

BACKGROUND: Photoperiodic control of development plays a key role in adaptation of plants to seasonal changes. A signaling module consisting of CONSTANS (CO) and FLOWERING LOCUS T (FT) mediates in photoperiodic control of a variety of developmental transitions (e.g., flowering, tuberization, and seasonal growth cessation in trees). How this conserved CO/FT module can mediate in the photoperiodic control of diverse unrelated developmental programs is poorly understood. RESULTS: We show that Like-AP1 (LAP1), a tree ortholog of Arabidopsis floral meristem identity gene APETALA1 (AP1), mediates in photoperiodic control of seasonal growth cessation downstream of the CO/FT module in hybrid aspen. Using LAP1 overexpressors and RNAi-suppressed transgenic trees, we demonstrate that short day (SD)-mediated downregulation of LAP1 expression is required for growth cessation. In contrast with AP1 targets in flowering, LAP1 acts on AINTEGUMENTA-like 1 transcription factor, which is implicated in SD-mediated growth cessation. Intriguingly, unlike AP1 in Arabidopsis, ectopic expression of LAP1 fails to induce early flowering in hybrid aspen trees. CONCLUSIONS: These results indicate that AP1 ortholog in trees has acquired a novel function in photoperiodic regulation of seasonal growth. Thus, photoperiodic signaling pathway may have diverged downstream of AP1/LAP1 rather than the CO/FT module during evolution. Moreover, control of flowering by the CO/FT module can be uncoupled from its role in photoperiodic control of seasonal growth in trees. Thus, our findings can explain mechanistically how a conserved signaling module can mediate in the control of a highly diverse set of developmental transitions by a similar input signal, namely photoperiod.