The trehalose 6‐phosphate pathway impacts vegetative phase change in Arabidopsis thaliana

Abstract

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.

Convergence and Divergence of Sugar and Cytokinin Signaling in Plant Development

“…This points to a cooperative regulation of root meristem activity by CK responses via miRNA156-targeted SPL10 [126]. Given that miRNA156 is a central component of sugar signaling [127], it will be of high interest to investigate whether sugars could take part in this regulatory network. CKs also cooperate with other hormones to regulate root meristem development.…”

Juvenile Leaves or Adult Leaves: Determinants for Vegetative Phase Change in Flowering Plants

“…Activation of TPS1 in an inducible line triggers downregulation of miR156. Interestingly, levels of sucrose, but not glucose nor fructose, are increased in transgenic plants with reduced activites of TPS1 [ 68 ]. The above results indicate that sugar promotes the adult phase by downregulating miR156.…”

Sugar Signaling and Post-transcriptional Regulation in Plants: An Overlooked or an Emerging Topic?

“…It is conserved in land plants and contributes to diverse physiological processes such as leaf development, heat stress memory, developmental transition, apical dominance, and flowering (Kim et al, 2012;Bhogale et al, 2014;Yu et al, 2015;Zhang, 2015;Gao et al, 2018;Kumar et al, 2020). The biological function of miRNA156 implies the repression of SQUAMOSA-PROMOTER BINDING PROTEIN-LIKEs (SPLs; Wang et al, 2009;Wahl et al, 2013;Xu et al, 2016;Wei et al, 2017;Zheng et al, 2019a,b;Hu et al, 2020, Jiao et al, 2020Ponnu et al, 2020). A direct link between sugar and miRNA156 abundance is based on the ability of exogenous glucose or sucrose supply to cause the levels of mature miRNA156 to drop and thereby accelerate the vegetative-reproductive phase transition, along with the juvenile-to-adult phase transition.…”

“…Conversely, defoliation and a reduced photosynthetic rate delay plant developmental transitions (Yang et al, 2013;Yu et al, 2013). The glucoseinduced repression of miRNA156 is dependent on the hexokinase 1-signaling pathway (Yang et al, 2013), while trehalose-6-phosphaste regulates developmental transition through a distinct mechanism (Wahl et al, 2013;Ponnu et al, 2020). miRNA156 also targets a variety of mRNAs that encode regulatory proteins involved in various physiological processes in plants (Wang and Wang, 2015).…”