Phytodetoxification of TNT by transgenic plants expressing a bacterial nitroreductase

Hannink, Nerissa K; Rosser, Susan J.; French, Christopher E.; Basran, Amrik; Murray, James A. H.; Nicklin, S.; Bruce, Neil C.

doi:10.1038/nbt1201-1168

Cited by 225 publications

(155 citation statements)

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“…One way this problem might be tackled is through the use of plants that are adapted to detoxify these compounds. This could be achieved either by traditional breeding programs or by genetic modification, as has been demonstrated previously for both RDX and TNT (Hannink et al, 2001;Rylott et al, 2006;Jackson et al, 2007).…”

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“…], and switchgrass [Panicum virgatum]), with the exception of some conifer trees (Schoenmuth and Pestemer, 2004), TNT is located almost entirely in the roots (Sens et al, 1998(Sens et al, , 1999Hannink et al, 2007;Van Dillewijn et al, 2008;Brentner et al, 2010). Endogenous metabolism of TNT by plants has been characterized Rylott et al, 2011b), with recent research focusing on the model plant species Arabidopsis (Arabidopsis thaliana; Hannink et al, 2001;Van Dillewijn et al, 2008;Rylott et al, 2011a). First, TNT is transformed by nitroreductases to hydroxylamino dinitrotoluenes (HADNTs), with a varying portion further reduced to amino dinitrotoluenes (ADNTs).…”

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“…In Arabidopsis, oxophytodienoate reductases are known to catalyze these steps (Beynon et al, 2009). Plants engineered to express bacterial nitroreductases, which also perform this transformation step, have increased TNT transformation activity and show dramatically enhanced resistance to TNT (Hannink et al, 2001;Rylott et al, 2011a). The additional functionality of HADNTs and ADNTs permits their subsequent conjugation to amino acids, organic acids, and sugars (Bhadra et al, 1999(Bhadra et al, , 2001, and conjugation of HADNT and ADNT isomers to Glc by Arabidopsis glucosyltransferases has been characterized (Gandia-Herrero et al, 2008), with research suggesting that these conjugates are subsequently sequestered within the cell walls .…”

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Arabidopsis Glutathione Transferases U24 and U25 Exhibit a Range of Detoxification Activities with the Environmental Pollutant and Explosive, 2,4,6-Trinitrotoluene

et al. 2014

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The explosive 2,4,6-trinitrotoluene (TNT) is a major worldwide military pollutant. The presence of this toxic and highly persistent pollutant, particularly at military sites and former manufacturing facilities, presents various health and environmental concerns. Due to the chemically resistant structure of TNT, it has proven to be highly recalcitrant to biodegradation in the environment. Here, we demonstrate the importance of two glutathione transferases (GSTs), GST-U24 and GST-U25, from Arabidopsis (Arabidopsis thaliana) that are specifically up-regulated in response to TNT exposure. To assess the role of GST-U24 and GST-U25, we purified and characterized recombinant forms of both enzymes and demonstrated the formation of three TNT glutathionyl products. Importantly, GST-U25 catalyzed the denitration of TNT to form 2-glutathionyl-4,6-dinitrotoluene, a product that is likely to be more amenable to subsequent biodegradation in the environment. Despite the presence of this biochemical detoxification pathway in plants, physiological concentrations of GST-U24 and GST-U25 result in only a limited innate ability to cope with the levels of TNT found at contaminated sites. We demonstrate that Arabidopsis plants overexpressing GST-U24 and GST-U25 exhibit significantly enhanced ability to withstand and detoxify TNT, properties that could be applied for in planta detoxification of TNT in the field. The overexpressing lines removed significantly more TNT from soil and exhibited a corresponding reduction in glutathione levels when compared with wild-type plants. However, in the absence of TNT, overexpression of these GSTs reduces root and shoot biomass, and although glutathione levels are not affected, this effect has implications for xenobiotic detoxification.The containment and cleanup of environmental pollutants is increasingly both a legal requirement and a responsible action in many developed countries. The most commonly used explosives in military weapons are 2,4,6-trinitrotoluene (TNT) and hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX), and their continual use, along with production and decommissioning, are progressively contaminating millions of hectares of military land . Bioremediation of TNT is particularly challenging, as the electron-withdrawing properties of the three nitro groups render the aromatic ring particularly resistant to oxidative attack and ring cleavage by microbial oxygenases, which in the environment are normally central to the biodegradation of aromatic compounds (Qasim et al., 2007). In the United States, the Environmental Protection Agency and the military are addressing methods by which toxic TNT and RDX can be contained and detoxified on active military training ranges. One way this problem might be tackled is through the use of plants that are adapted to detoxify these compounds. This could be achieved either by traditional breeding programs or by genetic modification, as has been demonstrated previously for both RDX and TNT (Hannink et al., 2001;Rylott et al., 2006;Jackson et al., 2007).In t...

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Arabidopsis Glutathione Transferases U24 and U25 Exhibit a Range of Detoxification Activities with the Environmental Pollutant and Explosive, 2,4,6-Trinitrotoluene

et al. 2014

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“…These enzymes are able to catalyze the reduction of the nitro group using and flavin mononucleotide (FMN) or flavin adenine dinucleotide (FAD) as a prosthetic group, and nicotinamide adenine dinucleotide (NAD(P)H) as reducing agent 16 . These proteins have attracted a great interest and environmental importance to human health, decreasing the toxicity of nitrocompounds, as well as, being applied in biotechnology, bioremediation and biocatalysis [17][18] . Studies report biotransformation of nitroaromatic compounds using Arracacia xanthorrhiza and Beta vulgaris associated with a microorganism Candida guilliermondii, coconut water which were converted into amines and to the corresponding acetamides.…”

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“…In recent years, plant parts and microorganisms have been related as a green alternative to reduce nitroaromatic compounds 9,17,21,23 . Therefore, in the order to find new sources of nitroreductases, we investigated the use the whole seeds of Linum usitatissimum L. for the bioreduction of nitroaromatic substrates (Scheme 1).…”

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Linseed (Linum usitatissimum L.) as a Biocatalyst for Reduction of Nitroaromatic Compounds

Tavares¹,

Lemos²,

Arriaga³

et al. 2014

Orient. J. Chem.

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Genes and Enzymes for In-Planta Phytoremediation of Air, Water and Soil

Schäffner¹,

Messner²,

Langebartels³

et al. 2002

Acta Biotechnol.

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SummaryPlants harbour highly versatile enzymatic machineries to attack and detoxify pollutants. Similarities to the mammalian detoxification led to the coining of the term "green liver" for plant xenobiotic metabolism. Important enzyme classes such as cytochrome P450 monoxygenases, glutathione S-transferases, glycosyltransferases and transporters are involved in both kingdoms. The availability of the first whole plant genome sequence of Arabidopsis thaliana revealed an unforeseen complexity of these enzyme classes. Genetic and biochemical diversity, by far exceeding at least single microorganisms, seems to exist in plants. In agreement with previous investigations at the enzymatic level both terrestrial and aquatic plants possess an enormous potential for phytoremediation of soil, water and air if limitations due to insufficient uptake into plants can be overcome. This is exemplified by the detoxification of herbicides, halogenated phenols and anilines, and formaldehyde by the action of plant enzymes. Two examples are discussed at the biochemical and genetic level. Plants can detoxify airborne formaldehyde by a glutathione-dependent formaldehyde dehydrogenase. Recombinant expression of an Arabidopsis UDP-glucose dependent glucosyltransferase showed activity towards both endogenous and xenobiotic substrates by a single enzyme. Plants frequently do not completely degrade xenobiotics, but rather form conjugated metabolites and "bound" residues. However, these potential contaminants can be easily removed by harvesting. In order to exploit this enormous potential of plants, promising approaches extending their endogenous capacity have been initiated. Transgenic organisms that express heterologous enzymes in order to specifically degrade compounds or to increase the mobility and uptake of recalcitrant xenobiotics are being pursued to make phytoremediation procedures useful in practice.

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Phytodetoxification of TNT by transgenic plants expressing a bacterial nitroreductase

Cited by 225 publications

References 19 publications

Arabidopsis Glutathione Transferases U24 and U25 Exhibit a Range of Detoxification Activities with the Environmental Pollutant and Explosive, 2,4,6-Trinitrotoluene

Arabidopsis Glutathione Transferases U24 and U25 Exhibit a Range of Detoxification Activities with the Environmental Pollutant and Explosive, 2,4,6-Trinitrotoluene

Linseed (Linum usitatissimum L.) as a Biocatalyst for Reduction of Nitroaromatic Compounds

Genes and Enzymes for In-Planta Phytoremediation of Air, Water and Soil

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