Interactions between metabolism and chromatin in plant models

Jörg Durner,Eva Esther Rudolf,Christian Lindermayr,Martin Groth

doi:10.1016/j.molmet.2020.01.015

Abstract

BackgroundOne 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 reviewThis 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 conclusionsDue 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.

Highlights

DNA is packaged inside eukaryotic nuclei by wrapping around histone proteins
Increased acetyl-CoA is accompanied by an increase in H3K27ac, which can result in altered aketoglutarate levels [26]. a-Ketoglutarate in turn is an important metabolic intermediate acting as cofactor for several chromatin-modifying enzymes [27]
This demonstrates how primary metabolism can affect chromatin structure, on the one side, and how these chromatin changes affect specific metabolic pathways, on the other side [26]. Such mutual relationships have to be addressed in more detail in the future, e.g. by time-course studies in combination with inducible inhibition/activation of genes/proteins involved in the production of redox molecules, cofactors, and other intermediates. It is presently well established in animals and plants that the levels of metabolic intermediates often globally correlate with the levels of epigenetic modifications for which they serve as cofactors

Summary

INTRODUCTION

DNA is packaged inside eukaryotic nuclei by wrapping around histone proteins. A total of 147 base pairs are fitted around each histone octamer consisting of two copies of each core histone H2A, H2B, H3, and H4. The enzymes that catalyze these modifications depend on metabolic intermediates as cosubstrates or cofactors This link between metabolism and epigenetic regulation is evident, the appreciation of the biological implications and underlying mechanisms has just begun. Adenosyl methionine, a-ketoglutarate, and acetyl-CoA, which are known to be required for chromatin modifications, it is likely that plants have evolved epigenetic mechanisms that integrate metabolic dynamics during development and environmental responses. Most insights are based on forward genetic screens aimed at the identification of gene silencing mechanisms and revealing many RNA and chromatin-associated factors, and components of metabolic pathways involved in cofactor regulation [8e12]. This review provides a comparison of current insights in the mammalian and plant fields Due to their prevalence and for the sake of space, we will focus on chromatin acetylation and methylation and the metabolism of the involved cofactors. We will put the described links between metabolism and chromatin dynamics in a biological context to discuss potential causes of environmentally induced epigenetic changes and how these changes might contribute to stress resistance in plants

HISTONE ACETYLATION AND ACETYL-COA METABOLISM

CHROMATIN METHYLATION AND ONE-CARBON METABOLISM

REDOX-DEPENDENT CHROMATIN MODULATION

CONCLUSIONS AND OUTLOOK