Grapevine cell response to carbon deficiency requires transcriptome and methylome reprogramming

Abstract

Sugar limitation has dramatic consequences on plant cells, which include cell metabolism and transcriptional reprogramming, and the recycling of cellular components to maintain fundamental cell functions. There is however no description of the contribution of epigenetic regulations to the adaptation of plant cells to limited carbon availability. We investigated this question using nonphotosynthetic grapevine cells (Vitis vinifera, cv Cabernet Sauvignon) cultured in vitro with contrasted glucose concentrations. Sugar depletion in the culture medium led to a rapid cell growth arrest and a major metabolic shift that include the depletion in soluble sugar and total amino acids and modulation of the cell redox status. Consistently, flux modeling showed a dramatic slowdown of many pathways required for biomass accumulation such as cell wall and protein synthesis. Sugar depletion 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, and at genes including some of those differentially expressed, consistent with an important role for methylation to 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 in plant cells under carbon shortage.

Acknowledgements

We are grateful to the genotoul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, https://doi.org/10.15454/1.5572369328961167E12) for providing advice, and giving access to computing facilities and storage resources.

Margot Berger was in receipt of a grant financed by CNIV (Comité National des Interprofessions du Vin) and by the Région Nouvelle Aquitaine (EPISTORE). Bernadette Rubio was in receipt of the PNDV (Plan National du dépérissement de la Vigne) funding EPIDEP. The work was supported by PNDV, Region Nouvelle Aquitaine and Bordeaux University.

Data availability

The data for this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB72068 (https://www.ebi.ac.uk/ena/browser/view/PRJEB72068).

Conflict of interest statement

The authors declare that they have no conflicts of interest.

Supplementary Data

Supplementary data are available at Horticulture Research online.

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