Abstract
Background Limitations in molecular oxygen reduce ATP production and dramatically curtail energy demanding processes in eukaryotes. Little is known of the influence of hypoxia on nuclear regulatory mechanisms and their integration with mRNA accumulation and translation. Here we apply multomic technologies to evaluate epigenetic to translational regulation in response to hypoxic stress in seedlings of Arabidopsis. We focus on hypoxia-responsive (HRG) and RIBOSOMAL PROTEIN (RP) genes that encode actively and poorly translated mRNAs under hypoxia, respectively.
Results Evaluation of hypoxia-induced dynamics in eight chromatin readouts including chromatin accessibility, histone modifications, RNA polymerase II (RNAPII) activity plus three RNA populations (nuclear, polyadenylated, and ribosome-associated) identified distinct patterns of nuclear regulation. HRGs coordinately increased promoter accessibility, Histone 2A.Z eviction, Histone 3-lysine 9 acetylation, and RNAPII engagement. Many HRG promoters were bound by HYPOXIA-RESPONSIVE ETHYLENE RESPONSIVE FACTOR (ERF) 2 (HRE2) or had cis-elements targeted by related ERFs. Hypoxia sustained RP transcription but the transcripts were largely retained in the nucleus. We discovered heat and oxidative stress genes with pronounced hypoxia-induced RNAPII engagement accompanied by elevated nuclear and ribosome-associated but not polyadenylated transcripts. These heat stress genes had cis-elements recognized by HEAT SHOCK FACTOR transcriptional activators, 5' biased histone marks, less H2A.Z eviction and Histone 3-lysine 4 trimethylation than genes bound by HRE2 and coordinately upregulated from transcription through translation. Genes of the circadian cycle, photosynthesis, and development also displayed notable nuclear regulation.
Conclusions Hypoxia triggers dominant patterns in nuclear regulatory control that differentiate cohorts of genes associated with stress responses and growth.