Oxygen Sensing via the Ethylene Response Transcription Factor RAP2.12 Affects Plant Metabolism and Performance under Both Normoxia and Hypoxia

Paul, Melanie; Iyer, Srignanakshi; Amerhauser, Carmen; Lehmann, Martin; Dongen, Joost T. van; Geigenberger, Peter

doi:10.1104/pp.16.00460

Cited by 89 publications

(81 citation statements)

References 43 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Suc exerts a very positive effect on Arabidopsis survival (Banti et al, 2008). Experiments using the 35S:D-RAP2.12 line demonstrated that constitutive expression of D-RAP2.12 results in stronger fermentative metabolism leading to lower carbohydrate availability and decreased tolerance to hypoxia (Paul et al, 2016). Tolerance was restored by feeding exogenous Suc, indicating that low levels of carbon reserves were the most likely reason for reduced anoxic resistance in 35S:D13RAP2.12 plants (Paul et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…The lower expression of DIN6, coding for an Asn synthase, observed in D-RAP2.12 and 35S: MA-RAP2.3 plants (Fig. 6) may reflect the altered amino acid metabolism in plants expressing a stable version of ERF-VII proteins (Paul et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…If so, induction of anaerobic genes would be detrimental, since the energy cost for producing the fermentative enzymes would not be compensated for by an effective additional ATP production in the absence of sugars as substrates. Similarly, plants submerged in conditions limiting photosynthesis will need to fine-tune induction of anaerobic genes to the level of available carbohydrates to avoid an excess amount of fermentative activity compromising survival (Paul et al, 2016). It is currently unknown if such a regulatory mechanism exist.…”

mentioning

confidence: 99%

See 2 more Smart Citations

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

et al. 2017

View full text Add to dashboard Cite

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

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

et al. 2017

View full text Add to dashboard Cite

show abstract

“…It controls mitochondrial respiration and TCA cycle enzymes, offering a genetic handle to adjust mitochondrial function when oxygen becomes limiting (Paul et al, 2016). RAP2.12 undergoes proteasome-mediated proteolysis through the N-end rule pathway under normoxic conditions and is protected from degradation under hypoxia (Gibbs et al, 2011;Licausi et al, 2011).…”

Section: Nitric Oxidementioning

confidence: 99%

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

et al. 2018

View full text Add to dashboard Cite

ORCID IDs: 0000-0001-5369-7911 (S.W.); 0000-0003-4024-968X (O.V.A.); 0000-0003-0796-8308 (M.S.).Cells of complex organisms typically rely on mitochondria for energy provision. The amount of energy required to sustain cellular activity can vary strongly depending on external conditions. Vice versa, constraints on respiratory activity due to metabolic status or stress insult require mitochondrial signaling to coordinate cellular physiology with the function of the organelle. In this update, we review recent insights into plant mitochondrial energy signaling in the light of their significance to stress acclimation. First, we focus on the characteristic adjustments of the nuclear transcriptome that occur after pharmacological inhibition of the mitochondrial electron transport chain as the output of mitochondrial retrograde signaling. Second, we discuss the proteins that have recently been identified as regulators of the transcript responses and the emerging picture of their action as a signaling network. We then pose the question of how well our current models of inducing mitochondrial dysfunction relate to conditions that plants face naturally. We reason that low-oxygen stress shows striking similarities with electron transport inhibitors with respect to their impact on mitochondrial energy physiology upstream, as well as the cellular transcriptomic response. Finally, we highlight and discuss changes in mitochondrial physiology that are common to both stimuli as candidates for upstream signals. The aim of this update is to better define the physiological context in which mitochondrial signaling operates to provide new directions for future research. RESPONSES TO MITOCHONDRIAL ENERGY SIGNALING AT THE TRANSCRIPT LEVEL

show abstract

“…Fermentation is an alternative pathway for the production of pyruvate under hypoxia, normally produced in the Krebs cycle, when oxygen is available. However, fermentation has disadvantages in relation to the aerobic pathway, such as lower ATP production, accumulation of toxic metabolites, and reduction in cytosolic pH (Paul et al, 2016). The accumulation of metabolites, like lactate, alcohol, alanine, succinate, and even malate, are markers of active metabolic pathways (van Dongen and Licausi, 2015;Paul et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Physiological Responses to Hypoxia and Manganese in Eucalyptus Clones with Differential Tolerance to Vale do Rio Doce Shoot Dieback

Harguindeguy

Castro

Novais

et al. 2018

Rev. Bras. Ciênc. Solo

View full text Add to dashboard Cite

ABSTRACT:Vale do Rio Doce shoot dieback (VRDSD) is an anomaly whose cause seems to be associated with hypoxic conditions and their consequences (excess Mn and Fe) triggered by elevation of the water table in areas with poor drainage. Different plants have distinct survival strategies under this form of stress. The objective of this study was to understand the physiological responses involved in the differential tolerance of eucalyptus clones to VRDSD and their relationship to hypoxia and excess Mn. A hydroponic experiment was carried out using a 2 × 2 × 2 factorial arrangement, two eucalyptus clones with different levels of tolerance to VRDSD (sensitive Urograndis hybrid -1213; and the tolerant Rio Claro hybrid -Eucalyptus grandis x unknown -2719), two concentrations of O 2 (8 and 4 mg L -1 ), and two Mn concentrations (1.39 and 300 mg L -1 ) in a randomized block design (RBD) with three replicates. Forty-day-old clones were maintained in Clark nutrient solution for 30 days. After this period, the treatments were applied for 11 days. Plant gaseous exchange shoot and root production, and the quantity of enzymes related to oxidative stress in leaves and roots were evaluated. In the tolerant clone, reactive oxygen species (ROS) were produced under hypoxic conditions, accompanied by reduction in production of dry matter, malondialdehyde (MDA), and in activity of the enzyme alcohol dehydrogenase (ADH). However, this clone had greater production of superoxide dismutase (SOD) under these conditions, an enzyme responsible for detoxification of ROS, which acts as part of the Low Oxygen Quiescence Syndrome (LOQS). In contrast, sensitive clones did not exhibit expressive reductions in growth or changes in the leaf/root ratio. These clones formed large quantities of adventitious roots and had high levels of MDA and ADH and low levels of SOD. Therefore, sensitive clones appear not to be prepared for detoxification of ROS and other toxic metabolites, but rather adopt morphological escape mechanisms, the Low Oxygen Escape Syndrome (LOES), in response to hypoxia. Thus, the period of soil waterlogging may cause the death of large numbers of roots in sensitive clones, limiting their ability to absorb water and nutrients and culminating in the death of these plants. Excess Mn seems to aggravate the damage caused by hypoxia, but it is not the causal agent of VRDSD.

show abstract

Oxygen Sensing via the Ethylene Response Transcription Factor RAP2.12 Affects Plant Metabolism and Performance under Both Normoxia and Hypoxia

Cited by 89 publications

References 43 publications

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

Physiological Responses to Hypoxia and Manganese in Eucalyptus Clones with Differential Tolerance to Vale do Rio Doce Shoot Dieback

Contact Info

Product

Resources

About