Autophagy Deficiency Compromises Alternative Pathways of Respiration following Energy Deprivation in Arabidopsis thaliana

Abstract

Under heterotrophic conditions, carbohydrate oxidation inside the mitochondrion is the primary energy source for cellular metabolism. However, during energy-limited conditions, alternative substrates are required to support respiration. Amino acid oxidation in plant cells plays a key role in this by generating electrons that can be transferred to the mitochondrial electron transport chain via the electron transfer flavoprotein/ubiquinone oxidoreductase system. Autophagy, a catabolic mechanism for macromolecule and protein recycling, allows the maintenance of amino acid pools and nutrient remobilization. Although the association between autophagy and alternative respiratory substrates has been suggested, the extent to which autophagy and primary metabolism interact to support plant respiration remains unclear. To investigate the metabolic importance of autophagy during development and under extended darkness, Arabidopsis () mutants with disruption of autophagy ( mutants) were used. Under normal growth conditions, mutants showed lower growth and seed production with no impact on photosynthesis. Following extended darkness, mutants were characterized by signatures of early senescence, including decreased chlorophyll content and maximum photochemical efficiency of photosystem II coupled with increases in dark respiration. Transcript levels of genes involved in alternative pathways of respiration and amino acid catabolism were up-regulated in mutants. The metabolite profiles of dark-treated leaves revealed an extensive metabolic reprogramming in which increases in amino acid levels were partially compromised in mutants. Although an enhanced respiration in mutants was observed during extended darkness, autophagy deficiency compromises protein degradation and the generation of amino acids used as alternative substrates to the respiration.

BZR1 Mediates Brassinosteroid-Induced Autophagy and Nitrogen Starvation in Tomato

“…Nutrient starvation induces the formation of autophagosomes to engulf the denatured proteins and transfer them to vacuoles for reuse, leading to enhanced N-utilization efficiency. However, autophagy-defective mutants compromise the degradation of proteins and the generation of amino acids (Barros et al, 2017). Similarly, BR treatment increased N uptake, which was associated with increased activity of nitrate reductase and increased levels of free amino acids and soluble proteins (Dalio et al, 2013).…”

Dual Role for Autophagy in Lipid Metabolism in Arabidopsis

“…Autophagy is functional at basal levels in virtually all cell types under favorable growth conditions but can also be massively induced by a wide array of developmental and environmental stimuli including nutrient starvation, senescence, pathogens, metabolic stress, and many other abiotic and biotic cues (Levine and Kroemer, 2008;Jaishy and Abel, 2016;Anding and Baehrecke, 2017;Wang et al, 2017;Nakamura and Yoshimori, 2018). The functional importance of both inducible and basal autophagy is well illustrated in plants using autophagy-defective mutants of Arabidopsis (Arabidopsis thaliana) and other plants (Liu et al, 2005;Guiboileau et al, 2012;Yoshimoto, 2012;Minina et al, 2014;Yang and Bassham, 2015;Barros et al, 2017;Üstün et al, 2017;Wang et al, 2017Wang et al, , 2018Elander et al, 2018;Enrique Gomez et al, 2018). These mutants display early senescence, shortened lifespan, reduced seed yield, defective reproductive growth, and altered phytohormone signaling under normal growth conditions and are also hypersensitive to nutrient deprivation, oxidative stress, pathogen infection, drought, and high salinity, although many mechanistic details underlying these phenotypes and the stress sensitivity remain largely unknown.…”

An additional role for chloroplast proteins—an amino acid reservoir for energy production during sugar starvation

“…Another study using a different set of autophagy-deficient mutants, atg5, atg7 and atg9, showed a lower increase in the levels of basic AAs, aromatic AAs and BCAAs in the atg plants than in wild-type plants during dark treatment. 15 These findings suggest a vital role for autophagy in the production of free AAs in response to sugar shortage.…”

“…In autophagy-deficient mutants, this response is impaired, resulting in an uncontrolled chloroplast degradation such as the strong activation of chloroplast vesiculation-containing vesicles (CCVs)-mediated pathway, 22 which is independent of autophagy, as previously suggested. 15 e1552057-2 chloroplast stroma-targeted autophagy during such stress conditions to better understand the survival strategies of plants. Numerous studies suggested the importance of autophagy in plant responses to various abiotic stresses, as well overviewed in a recent review.…”