Root growth in maize (Zea mays L.) is regulated by the activity of the quiescent center (QC) stem cells located within the root apical meristem. Here, we show that despite being highly hypoxic under normal
oxygen tension, QC stem cells are vulnerable to hypoxic stress, which causes their degradation with subsequent inhibition of root growth. Under low
oxygen, QC stem cells became depleted of
starch and soluble
sugars and exhibited reliance on glycolytic fermentation with the impairment of the TCA cycle through the depressed activity of several
enzymes, including
pyruvate dehydrogenase (PDH). This finding suggests that
carbohydrate delivery from the shoot might be insufficient to meet the metabolic demand of QC stem cells during stress. Some metabolic changes characteristic of the hypoxic response in mature root cells were not observed in the QC.
Hypoxia-responsive genes, such as
PYRUVATE DECARBOXYLASE (PDC) and
ALCOHOL DEHYDROGENASE (ADH), were not activated in response to
hypoxia, despite an increase in ADH activity. Increases in
phosphoenolpyruvate (PEP) with little change in steady-state levels of
succinate were also atypical responses to low-
oxygen tensions. Overexpression of PHYTOGLOBIN 1 (ZmPgb1.1) preserved the functionality of the QC stem cells during stress. The QC stem cell preservation was underpinned by extensive metabolic rewiring centered around activation of the TCA cycle and retention of
carbohydrate storage products, denoting a more efficient energy production and diminished demand for
carbohydrates under conditions where nutrient transport may be limiting. Overall, this study provides an overview of metabolic responses occurring in plant stem cells during
oxygen deficiency.