Temperature but not the circadian clock determines nocturnal carbohydrate availability for growth in cereals

Abstract

The circadian clock is considered a key target for crop improvement because it controls metabolism and growth in Arabidopsis. Here, we show that the clock gene EARLY FLOWERING 3 (ELF3) controls vegetative growth in Arabidopsis but not in the cereal crop barley. Growth in Arabidopsis is determined by the degradation of leaf starch reserves at night, which is controlled by ELF3. The vegetative growth of barley, however, is determined by the depletion of leaf sucrose stores through an exponential kinetics, presumably catalyzed by the vacuolar sucrose exporter SUCROSE TRANSPORTER 2 (SUT2). This process depends on the sucrose content and the nighttime temperature but not on ELF3. The regulation of starch degradation and sucrose depletion in barley ensures efficient growth at favorable temperature as stores become exhausted at dawn. On cool nights, however, only the starch degradation rate is compensated against low nighttime temperatures, whereas the sucrose depletion rate is reduced. This coincides with reduced biomass in barley but not in Arabidopsis after growth in consecutive cool nights. The sucrose depletion metabolism determines growth in the cereal crops barley, wheat, and rice but is not generally conserved in monocot species and is not a domestication-related trait. Therefore, the control of growth by endogenous (clock) versus external factors (temperature) is species-specific and depends on the predominant carbohydrate store. Our results give new insights into the physiology of growth in cereals and provide a basis for studying the genetics and evolution of different carbohydrate stores and their contribution to plant productivity and adaptation.\n\nSignificance StatementThe circadian clock controls growth in the model plant Arabidopsis thaliana by regulating the starch degradation rate so that reserves last until dawn. This prevents nocturnal starvation until photosynthesis resumes. The cereal crops barley, wheat and rice, however, predominantly consume sucrose instead of starch as carbohydrate source. We find that carbohydrate supply from sucrose at night is regulated by enzyme kinetics and night-time temperature, but not the circadian clock. We postulate that the regulation of growth depends on the predominant carbohydrate store, where starch degradation is controlled by endogenous cues (clock) and sucrose depletion by external factors (temperature). These differences in the regulation of carbohydrate availability at night may have important implications for adapting crops yields to climate change.