Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

Abstract

Plants respond to hypoxia, often caused by submergence, by expressing a specific set of genes that contribute to acclimation to this unfavorable environmental condition. Genes induced by low oxygen include those encoding enzymes for carbohydrate metabolism and fermentation, pathways that are required for survival. Sugar availability is therefore of crucial importance for energy production under hypoxia. Here, we show that Arabidopsis (Arabidopsis thaliana) plants require starch for surviving submergence as well as for ensuring the rapid induction of genes encoding enzymes required for anaerobic metabolism. The starchless pgm mutant is highly susceptible to submergence and also fails to induce anaerobic genes at the level of the wild type. Treating wild-type plants under conditions inducing sugar starvation results in a weak induction of alcohol dehydrogenase and other anaerobic genes. Induction of gene expression under hypoxia requires transcription factors belonging to group VII ethylene response factors (ERF-VII) that, together with plant Cys oxidases, act as an oxygen-sensing mechanism. We show that repression of this pathway by sugar starvation occurs downstream of the hypoxia-dependent stabilization of ERF-VII proteins and independently of the energy sensor protein kinases SnRK1

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

“…2b-c, 3c), it does not trigger accumulation of most hypoxia adaptive gene transcripts until hypoxia occurs (Supplementary Figure 5). Apparently, stabilization of ERFVIIs alone is insufficient to trigger full activation of hypoxia-regulated gene transcription and additional hypoxia-specific signals such as altered ATP and/or Ca 2+ levels are required 32–34 . The possible existence of undiscovered plant O 2 sensors was recently discussed and could potentially fulfil this role 35 .…”

Different ways to die in a changing world: Consequences of climate change for tree species performance and survival through an ecophysiological perspective

“…As fermentation generates approximately 16 times less energy than oxidative phosphorylation, an energy deficit is expected under flooding conditions, particularly if photosynthesis is also reduced. This energy imbalance can be partially overcome through consumption of reserve materials (e.g., nonstructural carbohydrates and lipids) and/or decreases in the activity of energy‐intensive processes (e.g., nitrogen (N) assimilation and cell wall formation; Christianson, Llewellyn, Dennis, & Wilson, ; Kolb, Rawyler, & Braendle, ; Kreuzwieser et al, ; Le Provost et al, ; Loreti, Valeri, Novi, & Perata). However, depending on the flooding duration, reserve consumption can lead to carbon deprivation, making the plant even more vulnerable to this and other stresses (e.g., high temperatures and pathogen attack).…”

“…Moreover, decreased reserve levels may also limit and/or increase the time required for a plant to fully recover its physiological activities (Li et al, 2015;Loreti et al, 2016), placing species inhabiting regions that undergo recurrent flooding events at even greater risk (Angelov et al, 1996). Thus, the ability to maintain a positive carbon balance appears to be one of the main determinants of the survival of species in flooding situations (Li et al, 2015;Loreti et al, 2018), even more so in a scenario that forecasts more frequent and intense flooding events (Lehmann, Coumou, & Frieler, 2015).…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…SnRK1-regulated endosperm starch catabolism is required to promote anaerobic metabolism during germination of rice seeds under extreme O 2 deficiency, and management of leaf starch catabolism is critical to submergence survival (Yu et al, 2015). The starchless plastidic PHOSPHOGLUCOMUTASE mutant was used in experiments that demonstrate a requirement for transitory leaf starch catabolism in submerged Arabidopsis rosettes that requires the ERF-VIIs but is independent of SnRK1 (Loreti et al, 2018).…”