Measuring and interpreting respiratory critical oxygen pressures in roots

Armstrong, W.; Webb, T.; Darwent, M. J.; Beckett, P. M.

doi:10.1093/aob/mcn177

Cited by 65 publications

(70 citation statements)

References 37 publications

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“…Here we show that the bigR operon in these pathogens, previously shown to influence bacterial biofilm formation (3), is required for hydrogen sulfide detoxification to allow bacterial growth under oxygen-limited conditions. Because hydrogen sulfide inhibits respiration, aerobic obligate bacteria such as Xylella and Agrobacterium must eliminate it to be able to grow under hypoxia, an environmental condition encountered by these pathogens in the interior of plant tissues (39,41,43). The data presented here indicate that hydrogen sulfide is oxidized to sulfite by the sulfur dioxygenase Blh and that sulfite, which is also toxic to the cells, is exported.…”

Section: Discussionmentioning

confidence: 79%

Plant Pathogenic Bacteria Utilize Biofilm Growth-associated Repressor (BigR), a Novel Winged-helix Redox Switch, to Control Hydrogen Sulfide Detoxification under Hypoxia

Guimarães¹,

Barbosa²,

Soprano

et al. 2011

Journal of Biological Chemistry

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Winged-helix transcriptional factors play important roles in the control of gene expression in many organisms. In the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens, the winged-helix protein BigR, a member of the ArsR/SmtB family of metal sensors, regulates transcription of the bigR operon involved in bacterial biofilm growth. Previous studies showed that BigR represses transcription of its own operon through the occupation of the RNA polymerase-binding site; however, the signals that modulate its activity and the biological function of its operon are still poorly understood. Here we show that although BigR is a homodimer similar to metal sensors, it functions as a novel redox switch that derepresses transcription upon oxidation. Crystal structures of reduced and oxidized BigR reveal that formation of a disulfide bridge involving two critical cysteines induces conformational changes in the dimer that remarkably alter the topography of the winged-helix DNA-binding interface, precluding DNA binding. This structural mechanism of DNA association-dissociation is novel among winged-helix factors. Moreover, we demonstrate that the bigR operon is required for hydrogen sulfide detoxification through the action of a sulfur dioxygenase (Blh) and sulfite exporter. As hydrogen sulfide strongly inhibits cytochrome c oxidase, it must be eliminated to allow aerobic growth under low oxygen tension, an environmental condition found in bacterial biofilms, xylem vessels, and root tissues. Accordingly, we show that the bigR operon is critical to sustain bacterial growth under hypoxia. These results suggest that BigR integrates the transcriptional regulation of a sulfur oxidation pathway to an oxidative signal through a thiol-based redox switch.Winged-helix proteins belong to a larger ensemble of helixturn-helix (HTH) 4 factors employed by living organisms to sense and respond to diverse environmental cues (1). For example, in bacterial cells, winged-helix transcriptional factors function as metal sensors, which control metal tolerance (2). In the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens, the winged-helix repressor protein BigR (biofilm growth-associated repressor) controls the expression of the bigR operon through the recognition of the Ϫ10 region in the operator site, thus blocking transcription of the operon genes (3). bigR operons are evolutionarily conserved in some plantassociated bacteria and human opportunistic pathogens and encode BigR itself, membrane transporters, and Blh, a DUF442-␤-lactamase domain protein related to the mitochondrial sulfur dioxygenase ETHE1 involved in sulfide detoxification in mammals (3, 4). Previous studies have shown that the bigR operon is actively transcribed in Xylella and Agrobacterium biofilms and that mutants lacking BigR can attach more tightly to glass and root surfaces than normal bacteria. Although these results strongly indicated that the bigR operon plays an important role in bacterial biofilm formation or cell adhesion, the biological function ...

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Section: Discussionmentioning

confidence: 79%

Plant Pathogenic Bacteria Utilize Biofilm Growth-associated Repressor (BigR), a Novel Winged-helix Redox Switch, to Control Hydrogen Sulfide Detoxification under Hypoxia

Guimarães¹,

Barbosa²,

Soprano

et al. 2011

Journal of Biological Chemistry

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“…Although O 2 levels were not completely depleted in nutrient solution, even after 24 h from hypoxia (Figure 1), the amount of O 2 that could be consumed by the roots is almost nil, as O 2 levels decrease at extremely low values and the diffusion rate in water is 10,000 times lower than in the air (Armstrong et al, 1994(Armstrong et al, , 2009Bailey-Serres et al, 2012).…”

Section: Discussionmentioning

confidence: 98%

Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes

Borella

Amarante

Oliveira

et al. 2014

Sci. agric. (Piracicaba, Braz.)

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Waterlogging blocks the oxygen supply to the root system which inhibits respiration, and greatly reduces the energy status of cells that affect important metabolic processes. This study evaluated fermentative metabolism and carbohydrate contents in the root system of two soybean (Glycine max L. Merril) genotypes under hypoxic and post-hypoxic conditions. Nodulated plants (genotypes Fundacep 53 RR and BRS Macota) were grown in vermiculite and transferred to a hydroponic system at the reproductive stage. The root system was submitted to hypoxia by flowing N 2 (nitrogen) gas in a solution for 24 and 72 h. For recovery, plants returned to normoxia condition by transfer to vermiculite for 24 and 72 h. Fermentative enzyme activity, levels of anaerobic metabolites and carbohydrate content were all quantified in roots and nodules. The activity of alcohol dehydrogenase, pyruvate decarboxylase and lactate dehydrogenase enzymes, as well as the content of ethanol and lactate, increased with hypoxia in roots and nodules, and subsequently returned to pre-hypoxic levels in the recovery phase in both genotypes. Pyruvate content increased in nodules and decreased in roots. Sugar and sucrose levels increased in roots and decreased in nodules under hypoxia in both genotypes. Fundacep RR 53 was more responsive to the metabolic effects caused by hypoxia and post-hypoxia than BRS Macota, and it is likely that these characteristics contribute positively to improving adaptation to oxygen deficiency.Keywords: Glycine max, oxygen deficiency, enzyme activities, anaerobic metabolites, sugars IntroductionSoil waterlogging is a common abiotic stress worldwide in cultivated areas and influences the composition and productivity of soybean (Glycine max L. Merril) and most crops species (Jackson and Colmer, 2005;Githiri et al., 2006;Sairam et al., 2009;Kokubun, 2013). In waterlogged soils, gas exchanges between root systems and soil porous spaces are limited due to oxygen diffusion resistance that is around 10,000 times higher in water than in the air (Armstrong et al., 1994;Dongen et al., 2003;Zabalza et al., 2009;Bailey-Serres et al., 2012).Decrease in the oxygen level is the main factor that causes stress, leading to a chain signaling that unleashes a series of metabolic changes (Horchani et al., 2009), such as N metabolism and interconversion of amino acids (Puiatti and Sodek, 1999;Oliveira et al., 2013), changes in carbohydrates levels and energetic metabolism (Sousa and Sodek, 2002a), in an effort to secure plant survival and growth when exposed to hypoxic stress (Geigenberger, 2003). Anaerobic metabolism is activated under low oxygen concentration and as a consequence, there is a significant decrease in energy production that is derived mainly from glycolysis in contrast to oxidative phosphorylation (Kumutha et al., 2008;Horchani et al., 2009;Sairam et al., 2009;Zabalza et al., 2009). Plant survival under these conditions depends almost exclusively on anaerobic metabolism (Sousa and Sodek, 2002a).Due to the lack of O 2 as the fi...

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“…Extensive work by Armstrong and others revealed various aspects of oxygen release by plant roots [16,[55][56][57][58]. Root oxygenation occurs in the daylight and depends to some extent on photosynthetic activity [59,60].…”

Section: Microclimatic Conditionsmentioning

confidence: 99%

Role of Plants in a Constructed Wetland: Current and New Perspectives

Shelef

Gross

Rachmilevitch

2013

Water

172

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Abstract:The role of plants in the treatment of effluents by constructed wetland (CW) systems is under debate. Here, we review ways in which plants can affect CW processes and suggest two novel functions for plants in CWs. The first is salt phytoremediation by halophytes. We have strong evidence that halophytic plants can reduce wastewater salinity by accumulating salts in their tissues. Our studies have shown that Bassia indica, a halophytic annual, is capable of salt phytoremediation, accumulating sodium to up to 10% of its dry weight. The second novel use of plants in CWs is as phytoindicators of water quality. We demonstrate that accumulation of H 2 O 2 , a marker for plant stress, is reduced in the in successive treatment stages, where water quality is improved. It is recommended that monitoring and management of CWs consider the potential of plants as phytoremediators and phytoindicators.

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Measuring and interpreting respiratory critical oxygen pressures in roots

Cited by 65 publications

References 37 publications

Plant Pathogenic Bacteria Utilize Biofilm Growth-associated Repressor (BigR), a Novel Winged-helix Redox Switch, to Control Hydrogen Sulfide Detoxification under Hypoxia

Plant Pathogenic Bacteria Utilize Biofilm Growth-associated Repressor (BigR), a Novel Winged-helix Redox Switch, to Control Hydrogen Sulfide Detoxification under Hypoxia

Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes

Role of Plants in a Constructed Wetland: Current and New Perspectives

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