Mitochondrial Sulfide Detoxification Requires a Functional Isoform O-Acetylserine(thiol)lyase C in Arabidopsis thaliana

Todhunter

Enviro Toxic and Chemistry

et al. 2017

The sensitivity of wild rice (Zizania palustris) to sulfide is not well understood. Because sulfate in surface waters is reduced to sulfide by anaerobic bacteria in sediments and historical information indicated that 10 mg/L sulfate in Minnesota (USA) surface water reduced Z. palustris abundance, the Minnesota Pollution Control Agency established 10 mg/L sulfate as a water quality criterion in 1973. A 21-d daily-renewal hydroponic study was conducted to evaluate sulfide toxicity to wild rice and the potential mitigation of sulfide toxicity by iron (Fe). The hydroponic design used hypoxic test media for seed and root exposure and aerobic headspace for the vegetative portion of the plant. Test concentrations were 0.3, 1.6, 3.1, 7.8, and 12.5 mg/L sulfide in test media with 0.8, 2.8, and 10.8 mg/L total Fe used to evaluate the impact of iron on sulfide toxicity. Visual assessments (i.e., no plants harvested) of seed activation, mesocotyl emergence, seedling survival, and phytoxicity were conducted 10 d after dark-phase exposure. Each treatment was also evaluated for time to 30% emergence (ET30), total plant biomass, root and shoot lengths, and signs of phytotoxicity at study conclusion (21 d). The results indicate that exposure of developing wild rice to sulfide at ≥3.1 mg sulfide/L in the presence of 0.8 mg/L Fe reduced mesocotyl emergence. Sulfide toxicity was mitigated by the addition of Fe at 2.8 mg/L and 10.8 mg/L relative to the control value of 0.8 mg Fe/L, demonstrating the importance of iron in mitigating sulfide toxicity to wild rice. Ultimately, determination of site-specific sulfate criteria taking into account factors that alter toxicity, including sediment Fe and organic carbon, are necessary. Environ Toxicol Chem 2017;36:2217-2226. © 2017 SETAC.

Section: Discussionmentioning

confidence: 99%

Toxicity of sulfide to early life stages of wild rice (Zizania palustris)

Todhunter

Enviro Toxic and Chemistry

et al. 2017

“…A possibility is that AOX activity is higher in the mutant (due to partial inhibition of cyt oxidase) and that the lower ATP yield is compensated by increasing the total electron flow to O 2 . Similarly, mutation of the mitochondrial OAS-C isoform resulted in accumulation of hydrogen sulfide and CN, accompanied again by increased AOX and higher total respiration rate [254]. Interestingly, both of the above mutants display a defect in root hair formation, suggesting a link between root hair initiation and the mitochondrion.…”

Section: Alternative Oxidase Plant Growth and Stress Tolerancementioning

confidence: 99%

Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants

Vanlerberghe

2013

IJMS

575

448

Alternative oxidase (AOX) is a non-energy conserving terminal oxidase in the plant mitochondrial electron transport chain. While respiratory carbon oxidation pathways, electron transport, and ATP turnover are tightly coupled processes, AOX provides a means to relax this coupling, thus providing a degree of metabolic homeostasis to carbon and energy metabolism. Beside their role in primary metabolism, plant mitochondria also act as “signaling organelles”, able to influence processes such as nuclear gene expression. AOX activity can control the level of potential mitochondrial signaling molecules such as superoxide, nitric oxide and important redox couples. In this way, AOX also provides a degree of signaling homeostasis to the organelle. Evidence suggests that AOX function in metabolic and signaling homeostasis is particularly important during stress. These include abiotic stresses such as low temperature, drought, and nutrient deficiency, as well as biotic stresses such as bacterial infection. This review provides an introduction to the genetic and biochemical control of AOX respiration, as well as providing generalized examples of how AOX activity can provide metabolic and signaling homeostasis. This review also examines abiotic and biotic stresses in which AOX respiration has been critically evaluated, and considers the overall role of AOX in growth and stress tolerance.

“…That is, the deficiency in energy production caused by the lack of a fully functional mETC could be partly compensated for by adequate provisioning in C source and cofactors, resulting in plantlets with reduced size and no roots. Although mutants affected in mitochondrial activity often exhibit global growth retardation (de Longevialle et al, 2007;García et al, 2010;Álvarez et al, 2012;Yuan and Liu, 2012;Zhu et al, 2012;Huang et al, 2013), the complete impairment of root development observed in cod1 mutants has not been documented so far. The origin of this inhibition is presently unclear but may result from the auxotrophic nature of root tissues or an insufficient induction of AOX activity in the roots or imbalanced mitochondrial ROS that are known to influence root formation (Gapper and Dolan, 2006).…”

Section: Cod1 Disruption Causes Embryo Development Arrest That Can Bementioning

confidence: 99%

Disruption of the CYTOCHROME C OXIDASE DEFICIENT1 Gene Leads to Cytochrome c Oxidase Depletion and Reorchestrated Respiratory Metabolism in Arabidopsis

et al. 2014

Cytochrome c oxidase is the last respiratory complex of the electron transfer chain in mitochondria and is responsible for transferring electrons to oxygen, the final acceptor, in the classical respiratory pathway. The essentiality of this step makes it that depletion in complex IV leads to lethality, thereby impeding studies on complex IV assembly and respiration plasticity in plants. Here, we characterized Arabidopsis (Arabidopsis thaliana) embryo-lethal mutant lines impaired in the expression of the CYTOCHROME C OXIDASE DEFICIENT1 (COD1) gene, which encodes a mitochondria-localized PentatricoPeptide Repeat protein. Although unable to germinate under usual conditions, cod1 homozygous embryos could be rescued from immature seeds and developed in vitro into slow-growing bush-like plantlets devoid of a root system. cod1 mutants were defective in C-to-U editing events in cytochrome oxidase subunit2 and NADH dehydrogenase subunit4 transcripts, encoding subunits of respiratory complex IV and I, respectively, and consequently lacked cytochrome c oxidase activity. We further show that respiratory oxygen consumption by cod1 plantlets is exclusively associated with alternative oxidase activity and that alternative NADH dehydrogenases are also up-regulated in these plants. The metabolomics pattern of cod1 mutants was also deeply altered, suggesting that alternative metabolic pathways compensated for the probable resulting restriction in NADH oxidation. Being the first complex IV-deficient mutants described in higher plants, cod1 lines should be instrumental to future studies on respiration homeostasis.