Abstract
Autophagic recycling of proteins, lipids, nucleic acids, carbohydrates, and organelles is essential for cellular homeostasis and optimal health, especially under nutrient-limiting conditions. To better understand how this turnover affects plant growth, development, and survival upon nutrient stress, we applied an integrated multiomics approach to study maize (Zea mays) autophagy mutants subjected to fixed-carbon starvation induced by darkness. Broad metabolic alterations were evident in leaves missing the core autophagy component ATG12 under normal growth conditions (e.g., lipids and secondary metabolism), while changes in amino acid-, carbohydrate-, and nucleotide-related metabolites selectively emerged during fixed-carbon starvation. Through combined proteomic and transcriptomic analyses, we identified numerous autophagy-responsive proteins, which revealed processes underpinning the various metabolic changes seen during carbon stress as well as potential autophagic cargo. Strikingly, a strong upregulation of various catabolic processes was observed in the absence of autophagy, including increases in simple carbohydrate levels with a commensurate drop in starch levels, elevated free amino acid levels with a corresponding reduction in intact protein levels, and a strong increase in the abundance of several nitrogen-rich nucleotide catabolites. Altogether, this analysis showed that fixed-carbon starvation in the absence of autophagy adjusts the choice of respiratory substrates, promotes the transition of peroxisomes to glyoxysomes, and enhances the retention of assimilated nitrogen.
Highlights
1! INTRODUCTION2! Plants employ a variety of adaptive responses to maintain adequate supplies of. 3! nutrients needed for growth, development, reproduction and stress protection, including
In starch levels, elevated free amino acid levels with a corresponding reduction in intact protein levels, and a strong increase in the abundance of several nitrogen-rich nucleotide catabolites. This analysis showed that fixed-carbon starvation in the absence of autophagy adjusts the choice of respiratory substrates, promotes the transition of peroxisomes to glyoxysomes, and enhances the retention of assimilated nitrogen
307! lipid droplet numbers were unaffected in wild type (0.54%) and only marginally reduced 308! in atg12 leaves (1.16%) when subjected to darkness (Figure 5A,B), either suggesting 309! that these lipid stores are not major respiratory substrates in the absence of fixed 310! carbon, or more likely, that they are in a dynamic equilibrium as membranes are 311! consumed and fed into respiration
Summary
2! Plants employ a variety of adaptive responses to maintain adequate supplies of. 3! nutrients needed for growth, development, reproduction and stress protection, including. 6! involves the autophagic turnover of intracellular proteins, lipids, carbohydrates, and. Kinase complex that decorates the autophagic membranes with a phosphatidylinositol-. That decorates phagophores and autophagosomes with ATG8 attached to the lipid. Strong hypersensitivity to nitrogen and fixed-carbon starvation Lipid metabolism and starch content, in part through defects in ER function, peroxisomal. Sativa) atg mutants have altered lipid and starch metabolism and plastid turnover, 82! Consistent with a role for autophagy in nutrient recycling, the mutant plants display. Autophagic clearance, thereby revealing the importance of autophagy in sculpting plant. Metabolism and lipid droplet breakdown associated with the atg mutations, we. Uncovered roles for autophagy in amino acid, carbohydrate, and starch metabolism, 108! 115! modify the carbon/nitrogen economy of maize and other crop species
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