Plants rely on sugars not only as energy sources but also as regulators of cellular activities. Carbon starvation disrupts central metabolism, impairs growth, and forces cells to recycle stored resources. Previous research has shown transcriptomic reprogramming and metabolic shifts under sugar depletion, but the contribution of epigenetic regulation—such as DNA methylation—remains poorly understood. Since methylation processes depend on metabolites like S-adenosyl-methionine, nutrient shortages may directly influence the epigenome. In animals and yeast, links between carbon metabolism and epigenetic changes are increasingly recognized. Due to these challenges, there is a pressing need to explore how plant cells coordinate metabolism and epigenetic regulation under carbon limitation.
A research team from the University of Bordeaux, INRAE, and collaborators published (DOI: 10.1093/hr/uhae277) their findings on September 28, 2024, in Horticulture Research. The study investigated how non-photosynthetic grapevine cells adapt to glucose deprivation. By integrating metabolomics, flux modeling, transcriptomics, and whole-genome bisulfite sequencing, the researchers uncovered how carbon starvation not only alters primary metabolism but also reshapes the DNA methylation landscape, thereby rewiring gene expression programs essential for survival.
The study used cultured grapevine (Vitis vinifera cv. Cabernet Sauvignon) cells exposed to glucose-rich and glucose-poor conditions. Within days of sugar depletion, cells stopped growing and displayed a marked metabolic shift: soluble sugars, proteins, and amino acids declined, while pathways involved in mobilizing stored resources became more active. Flux balance modeling confirmed reduced activity in glycolysis, the TCA cycle, and biomass synthesis, alongside increased mobilization of cell wall polymers and proteins.
Transcriptomic analysis identified over 5,600 differentially expressed genes, with stress-related and photosynthesis genes strongly induced, while those linked to cell cycle, translation, and biosynthesis were repressed. At the epigenetic level, whole-genome bisulfite sequencing revealed elevated global DNA methylation in sugar-starved cells, particularly in CHH and CHG sequence contexts. Nearly 850 differentially methylated regions were detected, many located in transposable elements but also in gene promoters. Strikingly, several transcription factors and metabolic enzymes showed coordinated shifts in promoter methylation and expression, suggesting that DNA methylation actively shapes transcriptional responses. Additional changes in histone modifier genes indicated that multiple layers of epigenetic regulation contribute to adaptation. Together, these results demonstrate that carbon starvation triggers an integrated reprogramming of metabolism, gene expression, and epigenetic states.
“Plants are masters of adaptation, and our work shows just how sophisticated these mechanisms can be,” said corresponding author Philippe Gallusci. “When deprived of sugar, grapevine cells don't simply slow down—they reorganize their metabolic priorities and remodel their epigenetic landscape. DNA methylation and histone modification act as molecular switches, coordinating which genes are turned on or off. This demonstrates that epigenetic regulation is central to plant resilience under stress, and it opens new avenues for understanding how crops respond to fluctuating carbon resources.”
These findings deepen our understanding of how plants integrate metabolic and epigenetic signals to survive energy shortages. For viticulture, insights into grapevine cell responses to carbon stress may shed light on berry development, sugar accumulation, and stress tolerance, all critical for fruit quality and wine production. More broadly, identifying epigenetic mechanisms that regulate adaptation could inform breeding and biotechnology strategies aimed at improving crop resilience. By linking carbon availability to methylome reprogramming, this research suggests that manipulating epigenetic pathways may one day help stabilize agricultural yields under nutrient stress and climate variability.
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References
DOI
10.1093/hr/uhae277
Original Source URL
https://doi.org/10.1093/hr/uhae277
Funding information
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.
About Horticulture Research
Horticulture Research is an open access journal of Nanjing Agricultural University and ranked number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2023. The journal is committed to publishing original research articles, reviews, perspectives, comments, correspondence articles and letters to the editor related to all major horticultural plants and disciplines, including biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.