Effects of glyphosate on metabolism of phenolic compounds II. Influence on soluble hydroxyphenolic compound, free amino acid and soluble protein levels in dark-grown maize roots

Hoagland, Robert E.; Duke, Stephen O.; Elmore, D. T.

doi:10.1016/0304-4211(78)90205-5

Cited by 31 publications

(35 citation statements)

References 14 publications

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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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confidence: 86%

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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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confidence: 86%

“…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.…”

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confidence: 99%

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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“…There have been reports on effects of glyphosate on the amino acid metabolism using axes of soybeans [Glycine max (L.) Merr.] (Duke et al, 1979(Duke et al, , 1980 and maize (Zea mays L.) (Hoagland et al, 1978), suspension-cultured cells of carrot (Daucus carota L.) and tobacco (Nicotiana tabacum L.) (Haderlie et al, 1977), rhizome buds of quackgrass [Elytrigia repens (L.) Nevski], roots of wheat (Triticum aestivum L.) (Cole et al, 1980), inflated duckweed (Lemna gibba L.) (Cooley and Foy, 1992). However, there is not any information on effects of glyphosate on the amino acid metabolism using floral organs.…”

Section: Introductionmentioning

confidence: 99%

Nitrogen Metabolism and Flower Symmetry of Petunia Corollas Treated with Glyphosate

Shimada

Kimura

2007

Zeitschrift Für Naturforschung C

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A change of flower shape was observed in petunia corollas treated with 0.5 mm glyphosate. Glyphosate changed the flower symmetry from the actinomorphic type to the zygomorphic type. Corollas treated with glyphosate showed an increased free amino acid content. Free amino acid profiles in petunia corollas revealed that glyphosate had no significant effect on aromatic amino acid levels but increased the level of proline. Soluble protein content in glyphosate-treated corollas did not cause any significant changes. The contents of soluble phenolics, lignin, and IAA in the corollas were not significantly affected by the glyphosate treatment. In contrast, glyphosate reduced the nitrate content and the RNA content of petunia corollas by 45% and 63% of the control, respectively. However, the DNA content in glyphosate-treated corollas was similar to that of the control.Low concentrations of glyphosate did not show any phytotoxic effects on the whole plants and any remarkable changes on aromatic amino acid metabolism and protein synthesis. However, glyphosate reduced the RNA content of petunia corollas and changed the flower symmetry from the actinomorphic type to the zygomorphic type. The results of nonprotein nitrogen metabolism in glyphosate-treated petunia corollas suggested that glyphosate application at low concentration may influence the regulation of flower symmetry through the change of RNA biosynthesis.

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“…It was also suggested (11) that glyphosate's effect on aromatic compounds may not be its principal mode of action. In the present HOLLANDER AND AMRHEIN study, we used an approach basically similar to that of Duke and Hoagland (9,16,17). We reasoned that, due to the possible functioning of a homeostatic control system and/or the possible involvement of more than one pool of aromatic amino acids (24), it might be difficult to detect a decreased level of a primary metabolite, such as phenylalanine, which, in addition, is likely to have a high turnover rate.…”

Section: Introductionmentioning

confidence: 99%

“…Nilsson (23) reported an increase in the amount of free amino acids and in NH3 in wheat plants sprayed with glyphosate, but the percentage of phenylalanine and tyrosine of the total amino acids was strongly reduced. In a series of recent papers, 16,17) hypothesized that glyphosate might exert its effect at least in part through induction of PAL4 activity, resulting in one or more of the following growth-limiting conditions: (a) depletion of free phenylalanine and, possibly, tyrosine levels and coincident inhibition of protein synthesis; (b) toxic levels of ammonia provided that the rate of deamination exceeds the rate of amination; and (c) accumulation of growth-limiting phenolics derived from trans-cinnamic acid, the product of the PAL reaction. In spite of the attractiveness of this proposal, there are alternative explanations for the induction of PAL by glyphosate (see under "Discussion"), and this hypothesis would not explain the growth-inhibitory action of glyphosate in organisms, such as bacteria, which do not have PAL.…”

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The Site of the Inhibition of the Shikimate Pathway by Glyphosate

Hollander¹,

Amrhein²

1980

Plant Physiol.

129

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The nonselective herbicide glyphosate (N-lphosphonomethyljglycine) 3 To whom reprint requests should be addressed.were added to the growth medium, but no effect of glyphosate was found on chorismate mutase, prephenate dehydrogenase, and prephenate dehydratase. High concentrations of the herbicide inhibited the two initial enzymes of the shikimate pathway, but this inhibition was apparently too slight to account for growth inhibition caused by low glyphosate concentrations. Inhibition by glyphosate of the growth of carrot and tobacco cells was alleviated by the addition of the three aromatic amino acids, but Haderlie et al. (15) hesitated to conclude that the synthesis of the aromatic amino acids was inhibited by glyphosate because glyphosate did not appreciably reduce the cellular concentrations of these amino acids. Just recently, Greshoff (14) extended the earlier studies of Jaworski (20) and Haderlie et al. (15) with an investigation on glyphosate's growth inhibition of E. coli, Chlamydomonas reinhardtii, carrot and soybean cell cultures, and Arabidopsis thaliana seedlings. In all cases, phenylalanine and tyrosine acted synergistically in the alleviation of the inhibitory effect of glyphosate. It was suggested that some essential process or compound derived from phenylalanine and/or tyrosine was inhibited by glyphosate or one of its metabolites (14). Nilsson (23) reported an increase in the amount of free amino acids and in NH3 in wheat plants sprayed with glyphosate, but the percentage of phenylalanine and tyrosine of the total amino acids was strongly reduced. In a series of recent papers, 16,17) hypothesized that glyphosate might exert its effect at least in part through induction of PAL4 activity, resulting in one or more of the following growth-limiting conditions: (a) depletion of free phenylalanine and, possibly, tyrosine levels and coincident inhibition of protein synthesis; (b) toxic levels of ammonia provided that the rate of deamination exceeds the rate of amination; and (c) accumulation of growth-limiting phenolics derived from trans-cinnamic acid, the product of the PAL reaction. In spite of the attractiveness of this proposal, there are alternative explanations for the induction of PAL by glyphosate (see under "Discussion"), and this hypothesis would not explain the growth-inhibitory action of glyphosate in organisms, such as bacteria, which do not have PAL. Furthermore, if conditions b or c were pertinent, one would expect that phenylalanine would increase the inhibitory effect of glyphosate rather than alleviate it.PAL, however, may contribute only partially to aromatic amino acid depletion, as was recently pointed out by Duke et al. (11). It was also suggested (11) that glyphosate's effect on aromatic compounds may not be its principal mode of action. In the present HOLLANDER AND AMRHEIN study, we used an approach basically similar to that of Duke and Hoagland (9,16,17). We reasoned that, due to the possible functioning of a homeostatic control system and/or the possible involvemen...

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Effects of glyphosate on metabolism of phenolic compounds II. Influence on soluble hydroxyphenolic compound, free amino acid and soluble protein levels in dark-grown maize roots

Cited by 31 publications

References 14 publications

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

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

Nitrogen Metabolism and Flower Symmetry of Petunia Corollas Treated with Glyphosate

The Site of the Inhibition of the Shikimate Pathway by Glyphosate

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