A temperature regime that disrupts clock-controlled starch mobilization induces transient carbohydrate starvation, resulting in compact growth

In nature, plants are usually subjected to a light/temperature regime of warm days and cold nights (referred to as +DIF). Compared with growth under +DIF, Arabidopsis plants show compact growth under the same photoperiod, but with an inverse temperature regime (cold days and warm nights: -DIF). Here we show that -DIF differentially affects the phase and amplitude of core clock gene expression. Under -DIF, the phase of the morning clock gene CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) is delayed, similar to that of plants grown on low sucrose. Indeed, under -DIF, carbohydrate (CHO) starvation marker genes are specifically up-regulated at the end of the night (EN) in Arabidopsis rosettes. However, only in inner rosette tissue (small sink leaves and petioles of older leaves) are sucrose levels lower under -DIF compared with under +DIF, suggesting that sucrose in source leaf blades is not sensed for CHO status and that sucrose transport from source to sink may be impaired at EN. CHO starvation under -DIF correlated with increased starch breakdown during the night and decreased starch accumulation during the day. Moreover, we demonstrate that different ways of inducing CHO starvation all link to reduced growth of sink leaves. Practical implications for control of plant growth in horticulture are discussed.