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.

Sugar Starvation Disrupts Lipid Breakdown by Inducing Autophagy in Embryonic Axes of Lupin (Lupinus spp.) Germinating Seeds

“…So, the enhanced expression of amino acid metabolism genes (Figure 5a,b) under such favorable trophic conditions is not surprising. Nevertheless, under nutrient depletion or starvation conditions, the increased demand for respiratory substrates occurs [44] and the acquisition of such substrates is remarkably easier from the degradation of storage protein than from storage lipid. If the source of respiratory and anabolic substrates is storage protein, amino acids are released from albumins and globulins (in lupins they are mainly globulins, constituting up to 80% of all storage proteins [1]) by the action of endo-and exopeptidases [20], and such amino acids are almost ready to supply the respiration.…”

Inactivation of mitochondrial complex IV inPhyscomitrium patensreveals the essential role of respiration in coordinating plants metabolism

“…Adenylate Energy Charge (AEC) was calculated as (ATP + ½ ADP) / (ATP + ADP + AMP) according to Tyutereva et al, 2022, based on the relative concentration of ATP, ADP and AMP obtained by IC-MS after normalization to the internal standard thio-ATP.…”

Mechanisms of Nutrient Uptake and Assimilation Processes in Some Plants: A Review

“…The carrier theory states that carriers encounter specific ions for which they have attraction, from carrier ion centres, and pass across membranes, then, the enzyme phosphatase situated at innermost membrane-bound increases, splits off phosphate from carrier complexes, and ions are discharged (Mengel and Kirkby, 1978;Alaoui et al, 2022). Marschner (1995) and (Tyutereva et al, 2022) observed that, in this transport process, energy is essential and participation of adenosine triphosphate (ATP) is usually rec ounted. Fageria et al (2006) and Griffiths and York (2020) reported that high energy molecule ATP is produced from adenosine diphosphate (ADP) = inorganic P (Pi) from respiration (oxidative phosphorylation reactions).…”