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Trehalose 6-phosphate (T6P), a trehalose synthesis intermediate and sugar phosphate, serves as a signaling molecule coordinating sucrose status with plant growth and development. Beyond its metabolic role, the T6P pathway integrates exogenous and other endogenous cues to regulate key developmental transitions, including embryogenesis, seed maturation and filling, shoot branching, vegetative and reproductive phase transitions, and tuber and lateral root formation. Dynamic spatiotemporal expression patterns of T6P-pathway genes correlate with developmental stages, though their specific contributions to the initiation and progression of these transitions remain under investigation. Here, we provide recent insights and future perspectives on the T6P pathway, emphasizing its role in orchestrating diverse plant developmental programs across model and crop species and highlighting emerging mechanistic insights into its functions.

The timing of flowering in plants is modulated by both carbon (C) and nitrogen (N) signaling pathways. In a previous study, we established a pivotal role of the sucrose-signaling trehalose 6-phosphate pathway in regulating flowering under N-limited short-day conditions. In this work, we show that both wild-type Arabidopsis (Arabidopsis thaliana) plants grown under N-limited conditions and knock-down plants of TREHALOSE PHOSPHATE SYNTHASE 1 induce FLOWERING LOCUS C (FLC) expression, a well-known floral repressor associated with vernalization. When exposed to an extended period of cold, a flc mutant fails to respond to N availability and flowers at the same time under N-limited and full-nutrition conditions. Our data suggest that SUCROSE NON-FERMENTING 1 RELATED KINASE 1-dependent trehalose 6-phosphate-mediated C signaling and a mechanism downstream of N signaling (likely involving NIN-LIKE PROTEIN 7) impact the expression of FLC. Collectively, our data underscore the existence of a multi-factor regulatory system in which the C and N signaling pathways jointly govern the regulation of flowering in plants.

Plant growth and development are regulated by many factors, including carbohydrate availability and signaling. Trehalose 6-phosphate (T6P), which is synthesized by TREHALOSE-6-PHOSPHATE SYNTHASE 1 (TPS1), is positively associated with and functions as a signal that informs the cell about the carbohydrate status. Mutations in TPS1 negatively affect the growth and development of Arabidopsis (Arabidopsis thaliana), and complete loss-of-function alleles are embryo-lethal, which can be overcome using inducible expression of TPS1 (GVG::TPS1) during embryogenesis. Using ethyl methane sulfonate mutagenesis in combination with genome re-sequencing, we have identified several alleles in the floral regulator gene HUA2 that restore flowering in tps1-2 GVG::TPS1. Genetic analyses using an HUA2 T-DNA insertion allele, hua2-4, confirmed this finding. RNA-seq analyses demonstrated that hua2-4 has widespread effects on the tps1-2 GVG::TPS1 transcriptome, including key genes and pathways involved in regulating flowering. Higher order mutants combining tps1-2 GVG::TPS1 and hua2-4 with alleles in the key flowering time regulators FLOWERING LOCUS T (FT), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), and FLOWERING LOCUS C (FLC) were constructed to analyze the role of HUA2 during floral transition in tps1-2 in more detail. Our findings demonstrate that loss of HUA2 can restore flowering in tps1-2 GVG::TPS1, in part through activation of FT, with contributions from the upstream regulators SOC1 and FLC. Interestingly, we found that mutation of FLC is sufficient to induce flowering in tps1-2 GVG::TPS1. Furthermore, we observed that mutations in HUA2 modulate carbohydrate signaling and that this regulation might contribute to flowering in hua2-4 tps1-2 GVG::TPS1.

Sensing carbohydrate availability is essential for plants to coordinate their growth and development. In Arabidopsis thaliana, TREHALOSE 6-PHOSPHATE SYNTHASE 1 (TPS1) and its product, trehalose 6-phosphate (T6P), are important for the metabolic control of development. tps1 mutants are embryo-lethal and unable to flower when embryogenesis is rescued. T6P regulates development in part through inhibition of SUCROSE NON-FERMENTING1 RELATED KINASE1 (SnRK1).

Here, we explored the role of SnRK1 in T6P-mediated plant growth and development using a combination of a mutant suppressor screen and genetic, cellular and transcriptomic approaches.

We report nonsynonymous amino acid substitutions in the catalytic KIN10 and regulatory SNF4 subunits of SnRK1 that can restore both embryogenesis and flowering of tps1 mutant plants. The identified SNF4 point mutations disrupt the interaction with the catalytic subunit KIN10.

Contrary to the common view that the two A. thaliana SnRK1 catalytic subunits act redundantly, we found that loss-of-function mutations in KIN11 are unable to restore embryogenesis and flowering, highlighting the important role of KIN10 in T6P signalling.

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.