Reactive oxygen species contribute to sugar signalling and growth in Arabidopsis

Roman A1,2, Deng D1, Eastmond H2, Arshad W2, Davey J2, James S2, Ashton PD2, Graham IA2 and Haydon MJ1,2

  1. School of BioSciences, The University of Melbourne, Parkville VIC.
  2. Department of Biology, University of York, UK.

Plants produce sugars from photosynthesis to provide the stored energy and building blocks for all living cells. Sugars also act as dynamic signals to regulate growth and physiology. Thus, carbon status has wide-ranging effects on plant productivity but defining specific sugar signalling pathways can be challenging in the context of photoautrophic metabolism because it is difficult to separate responses to light and sugar. We have previously shown that sugar signals regulate circadian rhythms in plants: exogenous sugars can initiate robust circadian rhythms in dark-grown seedlings; and inhibition of photosynthesis in the light can adjust phase of the circadian oscillator. To dissect contributions of sugar and light signals on gene networks in Arabidopsis, we have performed an RNA-Seq time-series in dark-adapted seedlings treated with sucrose or mannitol in the dark or transferred to the light with or without an inhibitor of photosynthesis. We have used weighted gene co-expression network analysis (WCGNA) and GO-enrichment of this large dataset to identify functional classes of transcripts. As expected, inhibition of photosynthesis identified GO-enrichment for ’circadian rhythm’ but also ’response to absence of light’, including transcripts for major photoreceptors. The latter suggests a contribution of sugars to canonical light signalling and indicates our experimental design could deconvolute light and sugar signals in plants. The most significantly-enriched class of transcripts responding early to sugar was ’response to oxygen-containing compound’, pointing to a potential role for reactive oxygen species (ROS) signalling. Using luciferase reporters and qPCR, we have shown that chemical inhibitors of ROS inhibit transcriptional responses to sugar. These inhibitors also inhibit promotive effects of sugars on root growth and shoot biomass, suggesting these contribute to meaningful sugar signalling pathways.