Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C

Abstract

Nutrients shape the growth, maturation, and aging of plants and animals. In plants, the juvenile to adult transition (vegetative phase change) is initiated by a decrease in miR156. In Arabidopsis, we found that exogenous sugar decreased the abundance of miR156, whereas reduced photosynthesis increased the level of this miRNA. This effect was correlated with a change in the timing of vegetative phase change, and was primarily attributable to a change in the expression of two genes, MIR156A and MIR156C, which were found to play dominant roles in this transition. The glucose-induced repression of miR156 was dependent on the signaling activity of HEXOKINASE1. We also show that the defoliation-induced increase in miR156 levels can be suppressed by exogenous glucose. These results provide a molecular link between nutrient availability and developmental timing in plants, and suggest that sugar is a component of the leaf signal that mediates vegetative phase change.

DOI: http://dx.doi.org/10.7554/eLife.00260.001

eLife digest

Like animals, plants go through several stages of development before they reach maturity, and it has long been thought that some of the transitions between these stages are triggered by changes in the nutritional status of the plant. Now, based on experiments with the plant Arabidopsis thaliana, Yang et al. and, independently, Yu et al. have provided fresh insights into the role of sugar in ‘vegetative phase change'—the transition from the juvenile form of a plant to the adult plant.

The new work takes advantage of the fact that vegetative phase change is controlled by two genes that encode microRNAs (MIRNAs). Arabidopsis has eight MIR156 genes and both groups confirmed that supplying plants with sugar reduces the expression of two of these— MIR156A and MIR156C—whereas sugar deprivation increases their expression. Removing leaves also leads to upregulation of both genes, and delays the juvenile to adult transition. Given that this effect can be partially reversed by providing the plant with sugar, it is likely that sugar produced in the leaves—or one of its metabolites—is the signal that triggers the juvenile to adult transition through the reduction of miR156 levels.

Consistent with this idea, Yang and co-workers revealed that mutant plants that are deficient in chlorophyll show elevated levels of miR156 and a delayed transition to the adult form. In addition, they showed that a gene called HXK1, which encodes a glucose signaling protein, helps to keep plants in the juvenile form under conditions of low sugar availability. HXK1 also contributes to the glucose-induced decrease in miR156 levels and does so, at least in part, by regulating the transcription of MIR156A and MIR156C genes into messenger mRNA. HXK1 is not solely responsible for the juvenile to adult transition, however, because plants that lack this protein are only slightly precocious in their transition to the adult form.

The works of Yang et al. and Yu et al. have thus provided key insights into the mechanisms by which a leaf-derived signal controls a key developmental change in plants. Just as fruit flies use their nutritional status to regulate the onset of metamorphosis, and mammals use it to control the onset of puberty, so plants use the level of sugar in their leaves to trigger the transition from juvenile to adult forms.

DOI: http://dx.doi.org/10.7554/eLife.00260.002