Interactions between metabolism and chromatin in plant models

Abstract

Background: One of the fascinating aspects of epigenetic regulation is that it provides means to rapidly adapt to environmental change. This is particularly relevant in the plant kingdom, where most species are sessile and exposed to increasing habitat fluctuations due to global warming. Although the inheritance of epigenetically controlled traits acquired through environmental impact is a matter of debate, it is well documented that environmental cues lead to epigenetic changes, including chromatin modifications, that affect cell differentiation or are associated with plant acclimation and defense priming. Still, in most cases, the mechanisms involved are poorly understood. An emerging topic that promises to reveal new insights is the interaction between epigenetics and metabolism.

Scope of review: This study reviews the links between metabolism and chromatin modification, in particular histone acetylation, histone methylation, and DNA methylation, in plants and compares them to examples from the mammalian field, where the relationship to human diseases has already generated a larger body of literature. This study particularly focuses on the role of reactive oxygen species (ROS) and nitric oxide (NO) in modulating metabolic pathways and gene activities that are involved in these chromatin modifications. As ROS and NO are hallmarks of stress responses, we predict that they are also pivotal in mediating chromatin dynamics during environmental responses.

Major conclusions: Due to conservation of chromatin-modifying mechanisms, mammals and plants share a common dependence on metabolic intermediates that serve as cofactors for chromatin modifications. In addition, plant-specific non-CG methylation pathways are particularly sensitive to changes in folate-mediated one-carbon metabolism. Finally, reactive oxygen and nitrogen species may fine-tune epigenetic processes and include similar signaling mechanisms involved in environmental stress responses in plants as well as animals.

Keywords: Chromatin; DNA methylation; Folate metabolism; Histone modification; Methionine cycle; Nitric oxide; Plants; Reactive oxygen species; Redox modification.

Figure 1

Folate-mediated C1 metabolism in Arabidopsis and its involvement in DNA and histone methylation. Enzymes with identified mutations that affect DNA and histone H3 lysine 9 methylation (5mC/K9m) in Arabidopsis are highlighted in red (further description and citations in main text). (1) Serine hydroxymethyltransferase (SHMT), (2) methylenetetrahydrofolate reductase (MTHFR), (3) methionine synthase (MS), (4) S-adenosylmethionine synthetase/methionine adenosyltransferase (SAMS/MAT), (5) DNA/histone methyltransferases, (6) S-adenosylhomocysteine hydrolase (SAHH), (7a) methylenetetrahydrofolate dehydrogenase, (7b) methenyltetrahydrofolate cyclohydrolase (7a&7b: MTHFD), (8) 10-formyltetrahydrofolate synthetase (10-FTHFS), (9) 10-formyltetrahydrofolate deformylase (10-FDF), (10) 5-formyltetrahydrofolate cycloligase (5-FCL), (11) glycine decarboxylase complex (GDC), (12) folylpolyglutamate synthetase (FPGS), THF(Glu₁) and THF refer to mono- and polyglutamylated tetrahydrofolate, respectively.

Figure 2

Model of stress interactions of metabolism and chromatin modification. Environmental stress leads to increased production of reactive oxygen species (ROS) and NO. ROS may lead to inactivation of DNA glycosylases involved in DNA demethylation (for example, ROS1). NO acts as an HDAC inhibitor and may also affect the activity of enzymes in the methionine (Met) cycle, for example, SAMS4 (1) and SAHH1 (2), leading to changes in SAM and SAH levels. This can lead to changes in histone lysine methylation (Kme) and cytosine methylation (5mC), as DNA methyltransferases (DNMTs) and histone methyltransferases (HMTs) require SAM as methyl donor and are inhibited by SAH. The Met cycle depends on C1 supply from the folate cycle.