Autophagy and the Energy Status of Plant Cells

Abstract

In plant cells the homeostatic control of energy balance involves the production and recycling of adenylates with macroergic bonds, ATP and ADP. The maintenance of anabolic processes requires the relative saturation of the adenylate pool with high energy phosphoanhydride bonds. The bulk of ATP synthesis is carried out both in mitochondria and in chloroplasts while optimal ATP levels within other cell compartments are maintained by adenylate kinases (AK). AK activity was recently found in cytosol, mitochondria, plastids and the nucleus. ATP synthesis in energy-producing organelles, as well as redistribution of nutrients among cellular compartments, requires fine-tuned regulation of ion homeostasis. A special role in energy metabolism is played by autophagy, a process of active degradation of unwanted and/or damaged cell components and macromolecules within the central lytic vacuole. So-called constitutive autophagy controls the quality of cellular contents under favorable conditions, i.e., when the cellular energy status is high. Energy depletion can lead to the activation of the pro-survival process of autophagic removal and utilization of damaged structures; the breakdown products are then used for ATP regeneration and de novo synthesis of macromolecules. Mitophagy and chlorophagy maintain the populations of healthy and functional energy-producing “stations”, preventing accumulation of defective mitochondria and chloroplasts as potential sources of dangerous reactive oxygen species. However, the increase of autophagic flux above a threshold level can lead to the execution of the vacuolar type of programmed cell death (PCD). In this case autophagy also contributes to preservation of energy through support of the outflow of nutrients from dying cells to healthy neighboring tissues. In plants, two central protein kinases, SnRK1 (Snf1-related protein kinase 1) and TOR (target of rapamycin), are responsible for the regulation of the metabolic switch between anabolic and catabolic pathways. TOR promotes the energy-demanding metabolic reactions in response to nutrient availability and simultaneously suppresses catabolism including autophagy. SnRK1, the antagonist of TOR, senses a decline in cellular energy supply and reacts by inducing autophagy through several independent pathways. Here, we provide an overview of the recent knowledge about the interplay between SnRK1 and TOR, autophagy and PCD in course of the regulation of energy balance in plants.