Unraveling the role of fermentation in the mode of action of acetolactate synthase inhibitors by metabolic profiling

Journal of Plant Physiology

Volumn 168, Issue 13, 2011, Pages 1568-1575

  Zabalza, Ana ^a,b   Orcaray, Luis ^a   Igal, María ^a   Schauer, Nicolas ^b,c   Fernie, Alisdair R ^b   Geigenberger, Peter ^d   van Dongen, Joost T ^b   Royuela, Mercedes ^a  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c Metabolomic Discoveries GmbH   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Acetolactate synthase inhibitors; Fermentation; Hypoxia; Imidazolinone; Metabolic profiling; Pyruvate

Indexed keywords

4 AMINOBUTYRIC ACID; ACETOLACTATE SYNTHASE; AMINO ACID; BRANCHED CHAIN AMINO ACID; HERBICIDE; IMAZETHAPYR; NICOTINIC ACID DERIVATIVE; OXYGEN; PUTRESCINE; PYRUVIC ACID;

ARTICLE; BIOSYNTHESIS; CELL HYPOXIA; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; MASS FRAGMENTOGRAPHY; METABOLISM; OXIDATION REDUCTION REACTION; PEA; PHYSIOLOGY; PLANT; PLANT ROOT; TIME;

ACETOLACTATE SYNTHASE; AMINO ACIDS; AMINO ACIDS, BRANCHED-CHAIN; CELL HYPOXIA; FERMENTATION; GAMMA-AMINOBUTYRIC ACID; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HERBICIDES; NICOTINIC ACIDS; OXIDATION-REDUCTION; OXYGEN; PEAS; PLANT ROOTS; PLANT SHOOTS; PUTRESCINE; PYRUVIC ACID; TIME FACTORS;

PISUM SATIVUM;

EID: 79959376376     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2011.02.015     Document Type: Article

References (36)

1. Bailey-Serres J., Chang R. Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann Bot 2005, 96:507-518.
2. Bestman H.D., Devine M.D., Vanden Born W.H. Herbicide chlorsulfuron decreases assimilate transport out of treated leaves of field pennycress (Thlaspi arvense L.) seedlings. Plant Physiol 1990, 93:1441-1448.
3. Das M., Reichman J.R., Haberer G., Welzl G., Aceituno F.F., Mader M.T., et al. A composite transcriptional signature differentiates responses towards closely related herbicides in Arabidopsis thaliana and Brassica napus. Plant Mol Biol 2010, 72:545-556.
4. Dolferus R., Jacobs M., Peacock W.J., Dennis E.S. Differential interactions of promoter elements in stress responses of the Arabidopsis adh gene. Plant Physiol 1994, 105:1075-1087.
5. Fernie A.R., Carrari F., Sweetlove L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 2004, 7:254-261.
6. Galvez L., Gonzalez E.M., Arrese-Igor C. Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 2005, 56:2551-2561.
7. Gaston S., Zabalza A., Gonzalez E.M., Arrese-Igor C., Aparicio-Tejo P.M., Royuela M. Imazethapyr, an inhibitor of the branched-chain amino acid biosynthesis, induces aerobic fermentation in pea plants. Physiol Plant 2002, 114:524-532.
8. Gaston S., Ribas-Carbo M., Busquets S., Berry J.A., Zabalza A., Royuela M. Changes in mitochondrial electron partitioning in response to herbicides inhibiting branched-chain amino acid biosynthesis in soybean. Plant Physiol 2003, 133:1351-1359.
9. Giardina M.C., Carosi S. Effects of chlorsulfuron on polyamine content in maize seedlings. Pest Biochem Physiol 1990, 36:229-236.
10. Gupta K.J., Zabalza A., van Dongen J.T. Regulation of respiration when the oxygen availability changes. Physiol Plant 2009, 137:383-391.
11. Kürsteiner O., Dupuis I., Kuhlemeier C. The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol 2003, 132:968-978.
12. Matsumura H., Miyachi S. Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol 1980, 69:465-470.
13. Millar A.H., Wiskich J.T., Whelan J., Day D.A. Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett 1993, 329:259-262.
14. Mohapatra S., Minocha R., Long S., Minocha S.C. Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids 2010, 38:1117-1129.
15. Narsai R., Rocha M., Geigenberger P., Whelan J., van Dongen J.T. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 2011, doi:10.1111/j.1469-8137.2010.03589.x.
16. Oliver S.N., Lunn J.E., Urbanczyk-Wochniak E., Lytovchenko A., van Dongen J.T., Faix B., et al. Decreased expression of cytosolic pyruvate kinase in potato tubers leads to a decline in pyruvate resulting in an in vivo repression of the alternative oxidase. Plant Physiol 2008, 148:1640-1654.
17. Orcaray L., Igal M., Marino D., Zabalza A., Royuela M. The possible role of quinate in the mode of action of glyphosate and acetolactate synthase inhibitors. Pest Manage Sci 2010, 66:262-269.
18. Reggiani R., Cantu C.A., BrambillaI, Bertani A. Accumulation and interconversion of amino acids in rice roots under anoxia. Plant Cell Physiol 1988, 29:981-987.
19. Reggiani R., Hochkoeppler A., Bertani A. Polyamines in rice seedlings under oxygen-deficit stress. Plant Physiol 1989, 91:1197-1201.
20. Rocha M., Licausi F., Araújo W.L., Nunes-Nesi A., Sodek L., Fernie A.R., et al. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 2010, 152:1501-1513.
21. Rocha M., Sodek L., Hameed M.W., Licausi F., Dornelas M.C., van Dongen J.T. Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 2010, 39:1043-1053.
22. Roessner U., Luedemann A., Brust D., Fiehn O., Linke T., Willmitzer L., et al. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 2001, 13:11-29.
23. Royuela M., Gonzalez A., Gonzalez E.M., Arrese-Igor C., Aparicio-Tejo P.M., Gonzalez-Murua C. Physiological consequences of continuous, sublethal imazethapyr supply to pea plants. J Plant Physiol 2000, 157:345-354.
24. Shaner D.L., Reider M.L. Physiological responses of corn (Zea mays) to AC 243,997 in combination with valine, leucine e isoleucine. Pest Biochem Physiol 1986, 25:248-257.
25. Shelp B.J., Bown A.W., McLean M.D. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 1999, 4:446-452.
26. Singh BK Biosynthesis of valine, leucine and isoleucine. Plant amino acids: biochemistry and biotechnology 1999, 227-247. Marcel Dekker, New York. B.K. Singh (Ed.).
27. Steinfath M., Strehmel N., Peters R., Schauer N., Groth D., Hummel J., et al. Discovering plant metabolic biomarkers for phenotype prediction using an untargeted approach. Plant Biotechnol J 2010, 8:900-911.
28. Trenkamp S., Eckes P., Busch M., Fernie A.R. Temporally resolved GC-MS-based metabolic profiling of herbicide treated plants reveals that changes in polar primary metabolites alone can distinguish herbicides of differing mode of action. Metabolomics 2009, 5:277-291.
29. Ulanov A., Lygin A., Duncan D., Widholm J., Lozovaya V. Metabolic effects of glyphosate change the capacity of maize culture to regenate plants. J Plant Physiol 2009, 166:978-987.
30. van Dongen J.T., Schurr U., Pfister M., Geigenberger P. Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 2003, 131:1529-1543.
31. van Dongen J.T., Fröhlich A., Ramirez-Aguilar S., Schauer N., Fernie A.R., Erban A., et al. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 2009, 103:269-280.
32. Wittenbach V.A., Abell L.M. Inhibition of valine, leucine and isoleucine biosynthesis. Plant amino acids: biochemistry and biotechnology 1999, 385-416. Marcel Dekker, New York. B.K. Singh (Ed.).
33. Zabalza A., Orcaray L., Gastón S., Royuela M. Carbohydrate accumulation in leaves of plants treated with the herbicide chlorsulfuron or imazethapyr is due to a decrease in sink strength. J Agric Food Chem 2004, 52:7601-7606.
34. Zabalza A., Gonzalez E.M., Arrese-Igor C., Royuela M. Fermentative metabolism is induced by inhibiting different enzymes of the branched-chain amino acid biosynthesis pathway in pea plants. J Agric Food Chem 2005, 53:7486-7493.
35. Zabalza A., Gaston S., Ribas-Carbó M., Orcaray L., Igal M., Royuela M. Nitrogen assimilation studies using 15N in soybean plants treated with imazethapyr, an inhibitor of branched-chain amino acid biosynthesis. J Agric Food Chem 2006, 54:8818-8823.
36. Zabalza A., van Dongen J.T., Froehlich A., Oliver S., Faix B., Kapuganti J.G., et al. Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 2009, 149:1087-1098.