Reversal of Glyphosate Inhibition of Carrot Cell Culture Growth by Glycolytic Intermediates and Organic and Amino Acids

Killmer, John L.; Widholm, Jack M.; Slife, F. W.

doi:10.1104/pp.68.6.1299

Cited by 27 publications

(15 citation statements)

References 24 publications

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“…Growth (8,9).Coupled with the use ofsuspension cultures, carbon-13 nuclear magnetic resonance (13C NMR) spectroscopy can provide an extremely powerful technique for characterizing metabolic reactions (2, 4, 13). Unlike carbon-14 studies which simply allow the determination of the extent of incorporation of a radiolabel into a given metabolite (after often extensive isolation, separation, and chromatographic purification of the metabolite), the use of specifically '3C-labeled substrates allows the fate of a specific carbon atom to be followed through many enzymic transformations of the original substrate.…”

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Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy

Ashworth¹,

Lee²,

Adams³

1987

Plant Physiol.

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ABSTRACrCarbon-13 nuclear magnetic resonance (NMR) spectroscopy has been applied to the direct observation of acetate and pyruvate metabolism in suspension cultures of Zea mays (var Black Mexican Sweet). Growth (8,9).Coupled with the use ofsuspension cultures, carbon-13 nuclear magnetic resonance (13C NMR) spectroscopy can provide an extremely powerful technique for characterizing metabolic reactions (2, 4, 13). Unlike carbon-14 studies which simply allow the determination of the extent of incorporation of a radiolabel into a given metabolite (after often extensive isolation, separation, and chromatographic purification of the metabolite), the use of specifically '3C-labeled substrates allows the fate of a specific carbon atom to be followed through many enzymic transformations of the original substrate. Not only the distribution of the label in the various intermediary metabolite pools of the cell but perhaps most importantly, the specific location ofthe labeled carbon atom in the various intermediate's molecular structure can be determined (15,16). This information can be obtained ' Present

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Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy

Ashworth¹,

Lee²,

Adams³

1987

Plant Physiol.

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“…In addition to the previously observed reversal of glyphosate inhibition by aromatic amino acids, it has been reported recently (12) (2), it was concluded that glyphosate may inhibit growth by causing ammonia to increase to toxic levels. Also, the tricarboxylic acid cycle indirectly feeds the shikimic acid pathway, and this cycle could be depleted by the rapid production of shikimic acid in the presence of glyphosate (1).…”

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“…In this paper, we report the effects of aspartate and other reversing agents (12) LSDo.os 9 rose for about 8 h, then leveled off at about 12 cpm iml-' in the presence of aspartate and about 20 cpm-ml-' in the absence of aspartate. Apparently, growth dilution was accompanied by a rapid reduction in net glyphosate uptake, and the longer term glyphosate content of the cells was determined largely during the first 8 h after inoculation.…”

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“…Also, the tricarboxylic acid cycle indirectly feeds the shikimic acid pathway, and this cycle could be depleted by the rapid production of shikimic acid in the presence of glyphosate (1). Killmer et al (12) proposed that organic acids could reverse glyphosate toxicity by preventing such a depletion. However, Jaworski (11) found that the shikimic acid precursors erythrose 4-phosphate and phosphoenolpyruvate failed to reverse glyphosate inhibition.…”

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Effects of Aspartate and Other Compounds on Glyphosate Uptake and Growth Inhibition in Cultured Carrot Cells

Nafziger

Widholm²,

Slife³

1983

Plant Physiol.

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The strong correlation between glyphosate uptake and growth inhibition of cultured carrot (Daucus carota L. cv Danvers) cells incubated in the presence ofaspartate suggests that aspartate reverses glyphosate inhibition of growth primarily by reducing intracellular glyphosate concentration. Other compounds which reverse glyphosate inhibition of cell growth gave a range of effects on glyphosate uptake: succinate, a-ketoglutarate, glutamate, pyruvate, and malate at 10 millimolar and phenylalanine at 2 millimolar reduced uptake by 0,8,11,16, 27, and 34%, respectively. These results suggest that more than one mechanism of reversal may operate in these cels.Glyphosate and aspartate produced only minor effects on intracellular ammonia, media pH, and cell viability. This suggests that ammonia toxicity may not be an inportant mechanism of action of glyphosate in this system.The activity of the nonselective herbicide glyphosate [N-(phos-phonomethyl)glycinel in plants has been under investigation for more than 10 years. Early work (11) showed that glyphosateinduced growth inhibition of duckweed (Lemna gibba) and Rhizobium japonicum could be overcome by supplying aromatic amino acids. Similar results have been reported with Escherichia coli, Chlamydomonas reinhardii, Arabidopsis thaliana, and cultured cells of carrot (Daucus carota), soybean (Glycine max), and tobacco (Nicotiana tabacum) (6,8).Based on the reversal of glyphosate inhibition by aromatic amino acids, it was proposed that the herbicide may act by reducing the synthesis of these amino acids (11). Glyphosateinduced reductions in the levels of aromatic amino acids have been found in maize roots (9), soybean hypocotyls (4), wheat (16), and buckwheat hypocotyls (10). Recent work (1) has shown that the reduction in aromatic amino acid levels may result from the inhibition of an enzyme in the pathway from shikimate to the aromatic amino acids. Using a cell-free extract from Aerobacter aerogenes, the enzyme 5-enolpyruvylshikimic-3-P synthetase was identified as the specific site of glyphosate inhibition (17). Similar activity in higher plants was inferred from the accumulation of shikimate and reductions in levels of its metabolites (e.g. chorismate and anthocyanin) in cultured Galium mollugo cells and in buckwheat hypocotyls (1).In addition to the previously observed reversal of glyphosate inhibition by aromatic amino acids, it has been reported recently (12) that a variety of organic and amino acids-pyruvic, a-ketoglutaric succinic, malic, glutamic, and aspartic-reverse glyphos-'This work was carried out with funds from the Illinois Agricultural Experiment Station and National Science Foundation Grant PCM 80-10927.ate inhibition of the growth of cultured carrot cells. From work showing that organic acids can reduce ammonia toxicity in cultured cells (2), it was concluded that glyphosate may inhibit growth by causing ammonia to increase to toxic levels. Also, the tricarboxylic acid cycle indirectly feeds the shikimic acid pathway, and this cycle could be dep...

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“…Furthermore, blockage of the shikimate pathway at EPSPS leads to deregulation of the pathway, resulting in accumulation of huge, possibly phytotoxic, concentrations of shikimate and benzoic acid derivatives of shikimate (Lydon and Duke, 1988). This deregulation and enhanced carbon flow into the shikimate pathway drains other biosynthetic pathways of necessary building blocks (Killmer et al, 1981;Jenson, 1985). Thus, the blockage of the shikimate pathway can lead to a large number of potentially damaging physiological effects.…”

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Herbicide-Resistant Field Crops

Dekker

Duke

1995

Advances in Agronomy

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This chapter reviews information about how crop plants resist herbicides and how resistance is selected for in plants and surveys specific herbicide-resistant crops by chemical family. The discussion in the chapter includes HRCs derived from both traditional and biotechnological selection methodologies. Plants avoid the effects of herbicides they encounter by several different mechanisms. These mechanisms can be grouped into two categories: those that exclude the herbicide molecule from the site in the plant where they induce the toxic response and those that render the specific site of herbicide action resistant to the chemical. The chapter presents herbicide-resistant crops by the herbicide chemical family-such as, triazine, acetolactate synthatase, acetyl-CoA carboxylase, glyphosate, bromoxynil, phenoxycarboxylic acids, and glufosinate. Resistant crops are listed in the chapter regardless of whether they have been commercialized or were developed for experimental purposes only, and are provided regardless of their "success" as resistant plants. DisciplinesAgricultural Science | Agriculture | Agronomy and Crop Sciences | Weed Science CommentsThis article is

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Reversal of Glyphosate Inhibition of Carrot Cell Culture Growth by Glycolytic Intermediates and Organic and Amino Acids

Cited by 27 publications

References 24 publications

Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy

Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy

Effects of Aspartate and Other Compounds on Glyphosate Uptake and Growth Inhibition in Cultured Carrot Cells

Herbicide-Resistant Field Crops

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Reversal of Glyphosate Inhibition of Carrot Cell Culture Growth by Glycolytic Intermediates and Organic and Amino Acids

Cited by 27 publications

References 24 publications

Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by 13C NMR Spectroscopy

Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by 13C NMR Spectroscopy

Effects of Aspartate and Other Compounds on Glyphosate Uptake and Growth Inhibition in Cultured Carrot Cells

Herbicide-Resistant Field Crops

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Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy

Characterization of Acetate and Pyruvate Metabolism in Suspension Cultures of Zea mays by ¹³C NMR Spectroscopy