Grapevine cell response to carbon deficiency requires transcriptome and methylome reprogramming

Sugar limitation has dramatic consequences on plant cells, which include a profound reorganization of the cell metabolism, transcriptional reprogramming, and the recycling of cellular components to maintain fundamental cell functions. There is so far no description of the possible contribution of epigenetic regulations in the adaptation of plant cells to limited carbon availability. We investigated this question using non-photosynthetic grapevine cells (Vitis vinifera, cv Cabernet Sauvignon) cultured in vitro with contrasted glucose concentrations. As expected, limited sugar availability in the culture medium led to a rapid cell growth arrest. This was associated with a major metabolic shift characterized by depletion in soluble sugar and total amino acids, an increase in malate content and changes in the cell redox status. Consistently, flux modeling showed a dramatic slowdown of many pathways required for biomass accumulation such as cell wall polymers and total protein content. In contrast, anaplerotic fluxes, the synthesis of some amino acids, redox and polyamine metabolism were enhanced. Carbon deprivation also resulted in a major transcriptional reprogramming characterized by the induction of genes involved in photosynthesis, and the repression of those related to sucrose mobilization or cell cycle control. Similarly, the epigenetic landscape was deeply modified. Glucose-depleted cells showed a higher global DNA methylation level than those grown with glucose. Changes in DNA methylation mainly occurred at transposable elements, but also at genes including differentially expressed genes, suggesting that DNA methylation could participate in the adaptation of cells to limited sugar availability. In addition, genes encoding histone modifiers were differentially expressed suggesting that additional epigenetic mechanisms may be at work during the response of plant cells to carbon shortage.