Global Analysis of the Role of Autophagy in Cellular Metabolism and Energy Homeostasis in Arabidopsis Seedlings under Carbon Starvation

Abstract

Germination and early seedling establishment are developmental stages in which plants face limited nutrient supply as their photosynthesis mechanism is not yet active. For this reason, the plant must mobilize the nutrient reserves provided by the mother plant in order to facilitate growth. Autophagy is a catabolic process enabling the bulk degradation of cellular constituents in the vacuole. The autophagy mechanism is conserved among eukaryotes, and homologs of many autophagyrelated (ATG) genes have been found in Arabidopsis thaliana. T-DNA insertion mutants (atg mutants) of these genes display higher sensitivity to various stresses, particularly nutrient starvation. However, the direct impact of autophagy on cellular metabolism has not been well studied. In this work, we used etiolated Arabidopsis seedlings as a model system for carbon starvation. atg mutant seedlings display delayed growth in response to carbon starvation compared with wild-type seedlings. High-throughput metabolomic, lipidomic, and proteomic analyses were performed, as well as extensive flux analyses, in order to decipher the underlying causes of the phenotype. Significant differences between atg mutants and wild-type plants have been demonstrated, suggesting global effects of autophagy on central metabolism during carbon starvation as well as severe energy deprivation, resulting in a morphological phenotype.

Roles for Light, Energy, and Oxygen in the Fate of Quiescent Axillary Buds

“…4). These findings suggest a requirement for alternative substrates to fuel the mitochondrial tricarboxylic acid pathway in the dark-treated condition (Araújo et al, 2012;Avin-Wittenberg et al, 2015).…”

A Central Role for Triacylglycerol in Membrane Lipid Breakdown, Fatty Acid β-Oxidation, and Plant Survival under Extended Darkness

“…A homolog of mammalian acid lipase in Arabidopsis has been shown to exhibit bono fide TAG lipase activity (El-Kouhen et al, 2005), but its role in TAG hydrolysis in nonseed tissues remains unknown. Autophagy plays a critical role in nutrient recycling in plants, and autophagic activity is induced during carbon starvations conditions (Izumi et al, 2013;Avin-Wittenberg et al, 2015). In future studies, it will be interesting to examine whether the autophagy-vacuole pathway contributes to TAG breakdown and fatty acid oxidation in plants.…”

Transitory Starch Metabolism in Guard Cells: Unique Features for a Unique Function

“…By carefully controlling the rate of starch degradation, the plant not only makes maximal use of its reserves for growth, but also avoids running out of carbon before the end of the night (Gibon et al, 2004). Premature exhaustion of starch reserves before dawn could trigger carbon starvation responses such as autophagy, resulting in loss of proteins and other cellular components that are metabolically expensive to replace, thereby having a negative impact on growth (Stitt and Zeeman, 2012;Avin-Wittenberg et al, 2015). We know from light-dark shift experiments and analysis of circadian clock mutants that the circadian clock plays a major role in this regulation, enabling the plant to predict the length of the coming night Graf and Smith, 2011).…”