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Selective mRNA translation coordinates energetic and metabolic adjustments to hypoxia and reoxygenation in Arabidopsis thaliana


Cellular oxygen deprivation (hypoxia/anoxia) requires an acclimation response that facilitates survival of an energy crisis. To gain new insights into the processes that enable endurance of transient low oxygen stress (LOS), dynamics in mRNA translation state and metabolites were quantitatively monitored in Arabidopsis thaliana seedlings exposed to a short (2 h) or prolonged (9 h) period of HS and following 1 h of reoxygenation. HS and reoxygenation promoted alterations in levels of polyribosomes (polysomes) that were highly coordinated with ATP content. The quantitative comparison of steady-state and polysomal mRNA populations revealed that over half of the cellular mRNAs displayed little or no change in abundance but were significantly restricted from ribosome complexes during HS. This selective translational repression was rapidly reversed upon reoxygenation. Comparison of the adjustment in gene transcripts and metabolites demonstrated that profiling of polysomal mRNAs strongly augments the prediction of cellular processes that are altered during hypoxia. This analysis reveals that the selective translation of a subset of mRNAs conserves ATP and facilitates the transition to anaerobic metabolism during low oxygen stress.