Oxygen Sensing and Integrative Stress Signaling in Plants

Schmidt, Romy; Weits, Daan A.; Feulner, Claudio F. J.; Dongen, Joost T. van

doi:10.1104/pp.17.01394

Cited by 90 publications

(82 citation statements)

References 105 publications

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“…Genes with expression ratios ≥2 and Padj <0.05 (n = 3) are depicted. Red and green boxes with arrows refer to the formerly reported categories of aerenchyma formation genes related to ethylene biosynthesis, RBOH, metallothionein, protein kinase and cell wall, based on 62,63,[87][88][89] •− which act as signalling molecules in this process 61 . In contrast with findings in Arabidopsis and rice, ethylene is not involved in early flood recognition and adaption to hypoxia in the tomato cultivar Moneymaker 14 .…”

Section: Hypoxia-induced Ros Production Redox Associated Gene Expresmentioning

confidence: 99%

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Safavi-Rizi

Herde

Stöhr

2020

Sci Rep

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Due to climate change, economically important crop plants will encounter flooding periods causing hypoxic stress more frequently. this may lead to reduced yields and endanger food security. As roots are the first organ to be affected by hypoxia, the ability to sense and respond to hypoxic stress is crucial. At the molecular level, therefore, fine-tuning the regulation of gene expression in the root is essential for hypoxia tolerance. Using an RnA-Seq approach, we investigated transcriptome modulation in tomato roots of the cultivar 'Moneymaker', in response to short-(6 h) and long-term (48 h) hypoxia. Hypoxia duration appeared to have a significant impact on gene expression such that the roots of five weeks old tomato plants showed a distinct time-dependent transcriptome response. We observed expression changes in 267 and 1421 genes under short-and long-term hypoxia, respectively. Among these, 243 genes experienced changed expression at both time points. We identified tomato genes with a potential role in aerenchyma formation which facilitates oxygen transport and may act as an escape mechanism enabling hypoxia tolerance. Moreover, we identified differentially regulated genes related to carbon and amino acid metabolism and redox homeostasis. Of particular interest were the differentially regulated transcription factors, which act as master regulators of downstream target genes involved in responses to short and/or long-term hypoxia. Our data suggest a temporal metabolic and anatomic adjustment to hypoxia in tomato root which requires further investigation. We propose that the regulated genes identified in this study are good candidates for further studies regarding hypoxia tolerance in tomato or other crops.

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Section: Hypoxia-induced Ros Production Redox Associated Gene Expresmentioning

confidence: 99%

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Safavi-Rizi

Herde

Stöhr

2020

Sci Rep

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“…cytosolic oxygenases, ER oxidoreductins that drive oxidative protein folding) that are not inhibited by AA. The concept of signal integration from various cellular compartments in low-oxygen signaling is reviewed by Schmidt et al (2018) as part of this Focus Issue. In the mitochondria, lack of oxygen will lead to efficient inhibition of electron transport flux without the backup by AOX, as in the case of AA.…”

Section: Low-oxygen Stress: Linking Our Insights From Models Of Mitocmentioning

confidence: 99%

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

et al. 2018

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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

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“…Their analysis complements the review by Schmidt et al (2018) that highlights integration of responses to O 2 deficiency, including consequences of mitochondrial electron transport inhibition and ROS release. We are reminded that there are more than 200 proteins that are putative targets of the O 2 -dependent N-end rule pathway responsible for ERF-VII turnover and more than 350 O 2 -dependent enzymes in Arabidopsis.…”

Section: Oxygen: Both Metabolic Necessity and Developmental Cuementioning

confidence: 99%

“…Updates in this issue consider how O 2 deficiency is managed through integrated signaling and response networks that reconfigure gene expression and metabolism and promote changes in anatomy or morphology that enhance aeration. These involve both direct and indirect sensing of changes in cellular O 2 homeostasis, with the latter involving the mitochondrion and both anterograde and retrograde signaling (Schmidt et al, 2018;Wagner et al, 2018). The low O 2 levels intrinsic to some developmental zones, such as meristems, also guide developmental processes in consort with light and carbon availability, as described for seasonal progressions in axillary buds (Signorelli et al, 2018).…”

Section: Oxygen: Both Metabolic Necessity and Developmental Cuementioning

confidence: 99%

“…We are reminded that there are more than 200 proteins that are putative targets of the O 2 -dependent N-end rule pathway responsible for ERF-VII turnover and more than 350 O 2 -dependent enzymes in Arabidopsis. The critical challenge of deciphering cellular dynamics in response to changing O 2 tension in a noninvasive manner for cellular and subcellular quantitation is discussed by Schmidt et al (2018).…”

Section: Oxygen: Both Metabolic Necessity and Developmental Cuementioning

confidence: 99%

See 1 more Smart Citation

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

Bailey‐Serres¹,

Pierik²,

Ruban³

et al. 2018

Plant Physiology

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Plants are exquisite in their capacity to convert photons of light through photosynthetic carbon dioxide (CO 2 ) fixation into carbohydrate resources that are assimilated and partitioned from photosynthetic source to sink tissues. The chemical energy gained from photosynthesis includes ATP and NADPH that along with sugars are vital to biosynthetic processes, cell proliferation, biomass production, and reproductive fitness. As in all eukaryotes, plants are dependent upon dioxygen (O 2 ) for efficient production of ATP through aerobic respiration by mitochondria. Therefore, O 2 is crucial for the efficient catabolism of carbohydrates, lipids, and protein into chemical energy in leaves in the light and darkness, as well as in sink tissues. In this Focus Issue, numerous reviews and research articles explore the integration of light, O 2 , and energy metabolism from the cellular to the whole-plant level. The articles analyze molecular, biochemical, physiological, and developmental mechanisms that contribute to the plant's energy balance. A recurrent theme is the integration of light, O 2 , and sugar sensing with signal transduction and gene regulation, resulting in metabolic and developmental plasticity that maximizes available energy for growth. This knowledge expands opportunities to enhance photosynthetic efficiency and finetune energy allocation to maximize yields of crops.

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Oxygen Sensing and Integrative Stress Signaling in Plants

Cited by 90 publications

References 105 publications

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

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

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

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