CARBON STARVED MAIZE MULTI-OMICS REVEAL ROLES FOR AUTOPHAGIC RECYCLING IN AMINO ACID, NUCLEOTIDE AND CARBOHYDRATE METABOLISM

Autophagic recycling of proteins, protein complexes, lipids, carbohydrates, and organelles is essential for cellular homeostasis and optimal growth, especially under nutrient-limiting conditions. To better understand how this turnover impacts plant growth, development and survival under nutrient stress, we applied a comprehensive multi-omic approach to study maize (Zea mays) autophagy mutants subjected to fixed-carbon starvation induced by darkness. Broad alterations the maize metabolome were evident in leaves missing the core autophagy component ATG12 (e.g., lipids and secondary metabolism) under normal growth conditions, while changes in amino acid-, carbohydrate- and nucleotide-related metabolites selectively emerged during fixed-carbon starvation. The metabolome changes during carbon stress were underpinned by substantial alterations of the maize leaf transcriptome and proteome, which exposed a strong upregulation of various catabolic processes in the absence of autophagic recycling. Included were increases in simple carbohydrates with a commensurate drop in starch indicative of energy deprivation, along with elevated amino acids and their precursors and several nitrogen-rich catabolites of nucleotides, suggestive of mis-regulated amino acid and nitrogen homeostasis. Through this integrated approach we identified several autophagy dependent and energy-related processes whose manipulation could be exploited to optimize crop yield.