Sweet Enough to Flower: In making the developmental switch from vegetative growth to flowering, plants integrate diverse information, including photoperiod, hormone signals, and carbohydrate status. Wahl et al. (p. 704 ; see the Perspective by Danielson and Frommer ) analyzed the physiology of the signaling sugar trehalose-6-phosphate (T6P) in Arabidopsis . Quantities of T6P cycle in daily rhythms that peak toward the end of the day. T6P levels in the shoot apical meristem mirrored sucrose levels. Disruption of T6P production also disrupted expression of the FLOWERING LOCUS T gene, which responds in leaves to day length and generates signals that direct the meristem to initiate flowering programs. T6P production also affected the signaling pathway that links the age of the plant to flowering. By incorporating requirements for T6P signaling in the flowering induction pathways, the plant ensures that adequate carbohydrate reserves have been accumulated. Thus, T6P regulates the shift to flowering by linking carbohydrate status to day length in the leaves and to developmental age in the shoot apical meristem.

Beyond their metabolic roles, sugars can also act as messengers in signal transduction. Trehalose, a sugar found in many species of plants and animals, is a non-reducing disaccharide composed of two glucose moieties. Its synthesis in plants is a two-step process, involving the production of trehalose-6-phosphate (T6P) catalyzed by trehalose-6-phosphate synthase (TPS) and its consecutive dephosphorylation to trehalose, catalyzed by trehalose-6-phosphate phosphatase (TPP). T6P has recently emerged as an important signaling metabolite, regulating carbon assimilation and sugar status in plants. In addition, T6P has also been demonstrated to play an essential role in plant development. This review recapitulates the recent advances we have made in understanding the role of T6P in coordinating diverse metabolic and developmental processes.

Significance: Plants adapt their growth and development to ambient light conditions by modulating the activity of the COP1/SPA ubiquitin ligase. In Arabidopsis , photoactivated cryptochromes interact directly with COP1/SPA to suppress the activity of COP1 in blue light. The molecular mechanisms of CRY-mediated inhibition of COP1 are not fully understood. Here we show that CRY2 inhibits COP1 by displacing degradation substrates from COP1. This mechanism requires a valine-proline (VP) motif present in the C-terminal domain of CRY2. These amino acids are also present in interactors of Arabidopsis and human COP1 and have been previously shown to directly bind the WD repeat of Arabidopsis and human COP1. Thus, the evolution of the plant-specific, VP-containing C-terminal domain of CRY2 might have allowed for light control of COP1 activity.

CONSTITUTIVE PHOTOMORPHOGENIC 1 functions as an E3 ubiquitin ligase in plants and animals. Discovered originally in Arabidopsis thaliana, COP1 acts in a complex with SPA proteins as a central repressor of light-mediated responses in plants. By ubiquitinating and promoting the degradation of several substrates, COP1/SPA regulates many aspects of plant growth, development and metabolism. In contrast to plants, human COP1 acts as a crucial regulator of tumorigenesis. In this review, we discuss the recent important findings in COP1/SPA research including a brief comparison between COP1 activity in plants and humans.

The ambient light environment controls many aspects of plant development throughout a plant9s life cycle. Such complex control is achieved because a key repressor of light signaling, the Arabidopsis COP1/SPA E3 ubiquitin ligase, causes the degradation of multiple regulators of endogenous developmental pathways. This includes the CONSTANS (CO) transcription factor which is responsible for photoperiodic control of flowering time. There are 16 CONSTANS-like proteins whose functions are only partly understood. Here, we show that 14 COL proteins bind COP1 and SPA1 in vitro. We subsequently focused on COL12 and show that COL12 binds COP1 and SPA proteins in vivo. The COL12 protein is degraded in darkness in a COP1-dependent fashion, indicating that COL12 is a substrate of the COP1/SPA ubiquitin ligase. Overexpression of COL12 causes late flowering specifically in long day conditions by decreasing the expression of FT. This phenotype is genetically dependent on CO. Consistent with this finding, COL12 physically interacts with CO in vivo, suggesting that COL12 represses flowering by inhibiting CO protein function. We show that COL12 overexpression did not alter CO protein stability. It is therefore likely that COL12 represses the activity of CO rather than CO levels. Overexpression of COL12 also affects plant architecture by increasing the number of rosette branches and reducing inflorescence height. These phenotypes are CO-independent. Hence, we suggest that COL12 affects plant development through CO-dependent and CO-independent mechanisms.

Summary: The vegetative phase change marks the beginning of the adult phase in the life cycle of plants and is associated with a gradual decline in the microRNA miR156, in response to sucrose status. Trehalose 6‐phosphate (T6P) is a sugar molecule with signaling function reporting the current sucrose state. To elucidate the role of T6P signaling in vegetative phase change, molecular, genetic, and metabolic analyses were performed using Arabidopsis thaliana loss‐of‐function lines in TREHALOSE PHOSPHATE SYNTHASE1 (TPS1), a gene coding for an enzyme that catalyzes the production of T6P. These lines show a significant delay in vegetative phase change, under both short and long day conditions. Induced expression of TPS1 complements this delay in the TPS1 knockout mutant (tps1‐2 GVG::TPS1). Further analyses indicate that the T6P pathway promotes vegetative phase transition by suppressing miR156 expression and thereby modulating the levels of its target transcripts, the SQUAMOSA PROMOTER BINDING PROTEIN‐LIKE genes. TPS1 knockdown plants, with a delayed vegetative phase change phenotype, accumulate significantly more sucrose than wild‐type plants as a result of a feedback mechanism. In summary, we conclude that the T6P pathway forms an integral part of an endogenous mechanism that influences phase transitions dependent on the metabolic state.