Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana

Abstract

SummaryCellular oxygen deprivation (hypoxia/anoxia) requires an acclimation response that enables survival during an energy crisis. To gain new insights into the processes that facilitate the endurance of transient oxygen deprivation, the dynamics of the mRNA translation state and metabolites were quantitatively monitored in Arabidopsis thaliana seedlings exposed to a short (2 h) or prolonged (9 h) period of oxygen and carbon dioxide deprivation and following 1 h of re-aeration. Hypoxia stress and reoxygenation promoted adjustments in the levels of polyribosomes (polysomes) that were highly coordinated with cellular ATP content. A quantitative comparison of steady-state and polysomal mRNA populations revealed that over half of the cellular mRNAs were restricted from polysome complexes during the stress, with little or no change in abundance. This selective repression of translation 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 cellular oxygen deprivation. The selective translation of a subset of mRNAs promotes the conservation of ATP and facilitates the transition to anaerobic metabolism during low-oxygen stress.

Regulation of poly(A) RNA retention in the nucleus as a survival strategy of plants during hypoxia

“…The use of the mRNA accumulated in the cell is supported by data showing only a 0.4% increase in total mRNA at 1 h after re-aeration, compared to an increase of more than 50% in mRNAs bound to ribosomes. 12 This result suggests that after the removal of stress, transcripts do not change much quantitatively or qualitatively. The strong growth in translation results from molecular processes leading to the transport of mRNA from the site of storage to the site of protein synthesis.…”

“…Storing a large amount of non-degraded transcript in the nucleus may be one of the causes of the strong decrease in translation in the absence of changes in the amount of mRNA. 11,12 Although our research shows a strong accumulation of poly (A) RNA in the cell nucleus, it does not concern all examined transcripts. In A. thaliana and Lupinus luteus, the mRNA of ADH1 did not stored in the cell nucleus during hypoxic stress.…”

“…9,10 Low O 2 conditions may result in a strong inhibition of protein synthesis by restricting ribosome association with the start codon of mRNA. 11 Branco-Price et al 12 show that this restriction applies to approximately 70% of cellular mRNA. This reduction in energy-consuming protein synthesis saves ATP, which is reduced by 50% after two hours of hypoxia.…”

“…A decrease in translation without a concurrent decrease in the number of transcripts occurred in approximately 50%. 12 The presence in the cytoplasm of stress granules (SG) rich in poly(A) RNA, might be the cellular expression of the inhibition of protein synthesis. The stress granules did not exhibit the presence of the translation initiation factors eIF2a; however, the presence of the 40S ribosomal subunit was shown in some of them.…”

A Short Period of Mannitol Stress but Not LiCl Stress Led to Global Translational Repression in Plants

“…2) Recent genome-scale analyses of translation have revealed that translational repression upon salinity stress and the other abiotic stresses can severely restrict gene expression and affect various mRNAs differently. [3][4][5] These findings suggest that global translational repression upon salinity stress is a major mechanism of gene expression control in the plant salinity stress response.…”