Metabolism of plant stem cells under low oxygen tension: metabolic reprogramming by phytoglobin (Pgb1) underlying stem cell functionality
The quiescent center (QC) stem cells of maize (Zea mays L.) roots are highly hypoxic under normal oxygen tension. Despite this state, they are vulnerable to hypoxic stress which causes their degradation with the subsequent inhibition of root growth. These effects are abolished by over-ever-expression of the nitric oxide (NO) scavenger Phytoglobin 1 (ZmPgb1.1) preserving the functionality of the QC stem cells during the stress. Among the metabolic changes occurring in WT QC stem cells under low oxygen are the depletion of starch and soluble sugars, reliance of glycolytic fermentation, and impairment of the TCA cycle through the depressed activity of several enzymes including pyruvate dehydrogenase (PDH). This suggests that carbohydrate delivery from the shoot is insufficient to meet the metabolic demand of the QC stem cells during the stress. Atypical hypoxic responses related to the induction of alcohol dehydrogenase (ADH) and accumulation of glycolytic metabolites were also identified.  The preservation of QC stem cells by ZmPgb1.1 was underpinned by extensive metabolic rewiring centered around to the activation of the TCA cycle and the retention of carbohydrate storage products, denoting a more efficient production of energy and diminished demand of carbohydrates under conditions where nutrient transport may be limiting. Overall, this study provides an unprecedented overview of metabolic responses occurring in plant stem cells during oxygen deficiency. Overall design: The roots of 5-day old maize (Zea mays L.) seedlings overexpressing [line ZmPgb1.1(S)] or down-regulating [line ZmPgb1.1(A)] Phytoglobin 1 (ZmPgb1.1) were exposed to normoxic (0h) and hypoxic conditions for 12 hours (12h). The quiescent center (QC) stem cells were isolated from the root tips for multi-omic measurements, including RNA-sequencing.