Conserved and nuanced hierarchy of gene regulatory response to hypoxia

Abstract

A dynamic assembly of nuclear and cytoplasmic processes regulate gene activity. Hypoxic stress and the associated energy crisis activate a plurality of regulatory mechanisms including modulation of chromatin structure, transcriptional activation and post-transcriptional processes. Temporal control of genes is associated with specific chromatin modifications and transcription factors. Genome-scale technologies that resolve transcript subpopulations in the nucleus and cytoplasm indicate post-transcriptional processes enable cells to conserve energy, prepare for prolonged stress and accelerate recovery. Moreover, the harboring of gene transcripts associated with growth in the nucleus and macromolecular RNA-protein complexes contributes to the preferential translation of stress-responsive gene transcripts during hypoxia. We discuss evidence of evolutionary variation in integration of nuclear and cytoplasmic processes that may contribute to variations in flooding resilience.

The Arabidopsis Calcium Sensor Calmodulin-like 38 Regulates Stress Granule Autophagy and Dynamics during Low Oxygen Stress and Re-aeration Recovery

“…Sorenson and Bailey-Serres, 2014), the hypoxia mRNA regulatory landscape is complex, and changes spatially and temporally depending upon the needs of the cell and the severity and duration of the energy stress (Cho et al, 2021;Lee and Bailey-Serres, 2021). The finding here that SG are targets of hypoxia-induced autophagy argues that this is part of the larger regulatory program that modulates mRNA homeostasis during long term hypoxia.…”

“…An example of exquisite cytosolic ribostatic control from higher plants is the reshuffling and reprograming of mRNA translation caused by flooding and submergence stress (Branco-Price et al, 2008;Mustroph et al, 2009;Juntawong et al, 2014;Lee and Bailey-Serres, 2021).…”

RNAi Mediated Hypoxia Stress Tolerance in Plants

“…The methylation of specific cytosines as well as the post-translational modifications of histones can increase or reduce the accessibility on gene regions. Studies on histone modification dynamics have shown how epigenetic modifications contribute to the regulation of HRG activation [ 18 , 20 ]. In Arabidopsis, the coding sequence of hypoxia-responsive genes is enriched in nucleosomes containing the repressive Histone 2A variant H2A.Z which makes the chromatin less accessible to the transcriptional complex.…”

“…These 49 hypoxia-responsive genes (HRGs) constitute the core of the anaerobic response in plants, and are efficiently and quickly transcribed, polyadenylated and translated upon low oxygen concentrations [ 18 , 19 ]. On the other hand, genes associated with growth and major cellular processes, including ribosomal protein genes (RPs) are constantly transcribed and polyadenylated; however, nuclear export and translation of their mRNAs are dampened until the tissues have been re-aerated [ 19 , 20 ].…”

Plant performance and food security in a wetter world

“…This is critical to understanding the dynamics and relevance of these signals during different flooded conditions and how their amalgamation generates distinct outputs. Simultaneously, we want to analyze across different tiers of gene regulation in a cell‐type specific way (Bailey‐Serres, 2013; Lee & Bailey‐Serres, 2021, in this issue). This will enable us to distinguish between low oxygen as a pre‐requisite for normal development and as a stress factor that hampers plant performance.…”