Amino Acids

, Volume 39, Issue 4, pp 933–947 | Cite as

Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress

  • Vijay Joshi
  • Je-Gun Joung
  • Zhangjun Fei
  • Georg Jander
Review Article


Pathways regulating threonine, methionine and isoleucine metabolism are very efficiently interconnected in plants. As both threonine and methionine serve as substrates for isoleucine synthesis, their synthesis and catabolism under different developmental and environmental conditions also influence isoleucine availability. Together, methionine gamma-lyase and threonine deaminase maintain the isoleucine equilibrium in plants under varied substrate availabilities. Isoleucine and the two other branched-chain amino acids (BCAAs) (leucine and valine) share four common enzymes in their biosynthesis pathways and thus are coordinately regulated. Induction of free amino acids as osmolytes in response to abiotic stress is thought to play a role in plant stress tolerance. In particular, the accumulation of BCAAs is induced many-fold during osmotic stress. However, unlike in the case of proline, not much research has been focused on understanding the function of the response involving BCAAs. This review describes pathways influencing branched-chain amino acid metabolism and what is known about the biological significance of their accumulation under abiotic stress. A bioinformatics approach to understanding the transcriptional regulation of the genes involved in amino acid metabolism under abiotic stress is also presented.


Methionine Threonine Isoleucine Abiotic stress Regulation 



This work was funded by grants from the National Science Foundation (MCB-0416567), the Binational Agriculture Research and Development Agency (US-3910-06) and the Triad Foundation to GJ, and National Science Foundation grants DBI-0501778 and DBI-0820405 to ZF.

Supplementary material

726_2010_505_MOESM1_ESM.pdf (27 kb)
Supplementary Table 1 (PDF 27 kb)
726_2010_505_MOESM2_ESM.pdf (20 kb)
Supplementary Table 2 (PDF 19 kb)
726_2010_505_MOESM3_ESM.pdf (240 kb)
Supplemental Figures 1 and 2 (PDF 239 kb)


  1. Ajjawi I, Lu Y, Savage LJ, Bell SM, Last RL (2009) Large scale reverse genetics in Arabidopsis: case studies from the Chloroplast 2010 Project. Plant Physiol. Epub ahead of print. doi: 10.1104/pp.109.148494
  2. Alia, Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200PubMedCrossRefGoogle Scholar
  3. Amir R (2010) Current understanding of the factors regulating methionine content in vegetative tissues of higher plants. Amino Acids (in press)Google Scholar
  4. Amir R, Hacham Y, Galili G (2002) Cystathionine gamma-synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends Plant Sci 7:153–156PubMedCrossRefGoogle Scholar
  5. Anderson MD, Che P, Song JP, Nikolau BJ, Wurtele ES (1998) 3-Methylcrotonyl coenzyme A carboxylase is a component of the mitochondrial leucine catabolic pathway in plants. Plant Physiol 118:1127–1138PubMedCrossRefGoogle Scholar
  6. Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482PubMedCrossRefGoogle Scholar
  7. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942PubMedCrossRefGoogle Scholar
  8. Bartlem D, Lambein I, Okamoto T, Itaya A, Uda Y, Kijima F, Tamaki Y, Nambara E, Naito S (2000) Mutation in the threonine synthase gene results in an over-accumulation of soluble methionine in Arabidopsis. Plant Physiol 123:101–110PubMedCrossRefGoogle Scholar
  9. Baum HJ, Madison JT, Thompson JF (1983) Feedback inhibition of homoserine kinase from radish leaves. Phytochemistry 22:2409–2412CrossRefGoogle Scholar
  10. Behl RK, Moawad AM, Achtnich W (1991) Amino acid and protein profile changes in a spring wheat mutant under prolonged heat stress. Ann Biol 7:63–68Google Scholar
  11. Binder S, Knill T, Schuster J (2007) Branched-chain amino acid metabolism in higher plants. Physiol Plant 129:68–78CrossRefGoogle Scholar
  12. Boerjan W, Bauw G, Vanmontagu M, Inze D (1994) Distinct phenotypes generated by overexpression and suppression of S-adenosyl-l-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6:1401–1414PubMedCrossRefGoogle Scholar
  13. Bourguignon J, Rebéillé F, Douce R (1998) Serine and glycine metabolism in higher plants. In: Singh BK (ed) Plant amino acids. Biochemistry & biotechnology. Marcel Dekker Inc., New York, pp 111–146Google Scholar
  14. Burg MB, Ferraris JD (2008) Intracellular organic osmolytes: function and regulation. J Biol Chem 283:7309–7313PubMedCrossRefGoogle Scholar
  15. Campalans A, Messeguer R, Goday A, Pages M (1999) Plant responses to drought, from ABA signal transduction events to the action of the induced proteins. Plant Physiol Biochem 37:327–340CrossRefGoogle Scholar
  16. Ceccarelli S, Grando S (1996) Drought as a challenge for the plant breeder. Plant Growth Regul 20:149–155CrossRefGoogle Scholar
  17. Chang AK, Duggleby RG (1998) Herbicide-resistant forms of Arabidopsis thaliana acetohydroxyacid synthase: characterization of the catalytic properties and sensitivity to inhibitors of four defined mutants. Biochem J 333:765–777PubMedGoogle Scholar
  18. Chipman D, Barak ZA, Schloss JV (1998) Biosynthesis of 2-aceto-2-hydroxy acids: acetolactate synthases and acetohydroxyacid synthases. Biochim Biophys Acta 1385:401–419PubMedGoogle Scholar
  19. Chuang DT, Shih VE (1995) Disorders of branched-chain amino acid and keto acid metabolism. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic basis of inherited disease, vol 1, 7th edn. McGraw-Hill, New York, pp 1239–1277Google Scholar
  20. Colau D, Negrutiu I, Van Montagu M, Hernalsteens JP (1987) Complementation of a threonine dehydratase-deficient Nicotiana plumbaginifolia mutant after Agrobacterium tumefaciens-mediated transfer of the Saccharomyces cerevisiae ILV1 gene. Mol Cell Biol 7:2552–2557PubMedGoogle Scholar
  21. Cornah JE, Germain V, Ward JL, Beale MH, Smith SM (2004) Lipid utilization, gluconeogenesis, and seedling growth in Arabidopsis mutants lacking the glyoxylate cycle enzyme malate synthase. J Biol Chem 279:42916–42923PubMedCrossRefGoogle Scholar
  22. Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S (2004) NASCArrays: a repository for microarray data generated by NASC’s transcriptomics service. Nucl Acids Res 32:D575–D577PubMedCrossRefGoogle Scholar
  23. Curien G, Dumas R, Ravanel S, Douce R (1996) Characterization of an Arabidopsis thaliana cDNA encoding an S-adenosylmethionine-sensitive threonine synthase. Threonine synthase from higher plants. FEBS Lett 390:85–90PubMedCrossRefGoogle Scholar
  24. Curien G, Ravanel S, Dumas R (2003) A kinetic model of the branch-point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana. Eur J Biochem 270:4615–4627PubMedCrossRefGoogle Scholar
  25. Curien G, Bastlen O, Robert-Genthon M, Cornish-Bowden A, Cardenas ML, Dumas R (2009) Understanding the regulation of aspartate metabolism using a model based on measured kinetic parameters. Mol Sys Biol 5:271. doi: 10.1038/msb.2009.29 Google Scholar
  26. Dancs G, Kondrak M, Banfalvi Z (2008) The effects of enhanced methionine synthesis on amino acid and anthocyanin content of potato tubers. BMC Plant Biol 8:65. doi: 10.1186/1471-2229-8-65 PubMedCrossRefGoogle Scholar
  27. de Kraker JW, Luck K, Textor S, Tokuhisa JG, Gershenzon J (2007) Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine. Plant Physiol 143:970–986PubMedCrossRefGoogle Scholar
  28. De Veylder L, Segers G, Glab N, Van Montagu M, Inze D (1997) Identification of proteins interacting with the Arabidopsis Cdc2aAt protein. J Exp Bot 48:2113–2114CrossRefGoogle Scholar
  29. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223CrossRefGoogle Scholar
  30. Deuschle K, Funck D, Forlani G, Stransky H, Biehl A, Leister D, van der Graaff E, Kunzee R, Frommer WB (2004) The role of delta(1)-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425PubMedCrossRefGoogle Scholar
  31. Dias B, Weimer B (1998) Conversion of methionine to thiols by Lactococci, Lactobacilli, and Brevibacteria. App Environ Microbiol 64:3320–3326Google Scholar
  32. Didion T, Grauslund M, KiellandBrandt MC, Andersen HA (1996) Amino acids induce expression of BAP2, a branched-chain amino acid permease gene in Saccharomyces cerevisiae. J Bact 178:2025–2029PubMedGoogle Scholar
  33. Diebold R, Schuster J, Daschner K, Binder S (2002) The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol 129:540–550PubMedCrossRefGoogle Scholar
  34. Duggleby RG, Pang SS (2000) Acetohydroxyacid synthase. J Biochem Mol Biol 33:1–36Google Scholar
  35. Dumas R, Job D, Ortholand JY, Emeric G, Greiner A, Douce R (1992) Isolation and kinetic-properties of acetohydroxy acid isomeroreductase from spinach (Spinacia oleracea) chloroplasts overexpressed in Escherichia coli. Biochem J 288:865–874PubMedGoogle Scholar
  36. Durner J, Boger P (1988) Acetolactate synthase from barley (Hordeum vulgare L.)—purification and partial characterization. Zeitschrift Fur Naturforschung 43:850–856Google Scholar
  37. Durner J, Boger P (1990) Oligomeric forms of plant acetolactate synthase depend on flavin adenine-dinucleotide. Plant Physiol 93:1027–1031PubMedCrossRefGoogle Scholar
  38. Eden A, Benvenisty N (1998) Characterization of a branched-chain amino-acid aminotransferase from Schizosaccharomyces pombe. Yeast 14:189–194PubMedCrossRefGoogle Scholar
  39. Faleev NG, Troitskaya MV, Paskonova EA, Saporovskaya MB, Belikov VM (1996) l-Methionine-gamma-lyase in Citrobacter intermedius cells: stereochemical requirements with respect to the thiol structure. Enzyme Microb Technol 19:590–593CrossRefGoogle Scholar
  40. Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18:1157–1161PubMedCrossRefGoogle Scholar
  41. Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7:899–906PubMedCrossRefGoogle Scholar
  42. Gao F, Wang CZ, Wei CH, Li Y (2009) A branched-chain aminotransferase may regulate hormone levels by affecting KNOX genes in plants. Planta 230:611–623PubMedCrossRefGoogle Scholar
  43. Garcia EL, Mourad GS (2004) A site-directed mutagenesis interrogation of the carboxy-terminal end of Arabidopsis thaliana threonine dehydratase/deaminase reveals a synergistic interaction between two effector-binding sites and contributes to the development of a novel selectable marker. Plant Mol Biol 55:121–134PubMedCrossRefGoogle Scholar
  44. Gerbling H, Gerhardt B (1989) Peroxisomal degradation of branched-chain 2-oxo acids. Plant Physiol 91:1387–1392PubMedCrossRefGoogle Scholar
  45. Goddard NJ, Dunn MA, Zhang L, White AJ, Jack PL, Hughes MA (1993) Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, BLT101. Plant Mol Biol 23:871–879PubMedCrossRefGoogle Scholar
  46. Gonda I, Bar E, Portnoy V, Lev S, Burger J, Schaffer AA, Tadmor Y, Gepstein S, Giovannoni JJ, Katzir N, Lewinsohn E (2010) Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. fruit. J Exp Bot. Epub ahead of printGoogle Scholar
  47. Good AG, Zaplachinski ST (1994) The effects of drought stress on free amino-acid accumulation and protein-synthesis in Brassica napus. Physiol Plant 90:9–14CrossRefGoogle Scholar
  48. Goyer A, Collakova E, Shachar-Hill Y, Hanson AD (2007) Functional characterization of a methionine gamma-lyase in Arabidopsis and its implication in an alternative to the reverse trans-sulfuration pathway. Plant Cell Phys 48:232–242CrossRefGoogle Scholar
  49. Graham IA, Eastmond PJ (2002) Pathways of straight and branched chain fatty acid catabolism in higher plants. Progr Lipid Res 41:156–181CrossRefGoogle Scholar
  50. Gu L, Daniel Jones A, Last RL (2009) Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J. Epub ahead of printGoogle Scholar
  51. Hacham Y, Matityahu I, Schuster G, Amir R (2008) Overexpression of mutated forms of aspartate kinase and cystathionine γ-synthase in tobacco leaves resulted in the high accumulation of methionine and threonine. Plant J 54(2):260–271PubMedCrossRefGoogle Scholar
  52. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  53. Heap I (2009) International survey of herbicide resistant weeds. Retrieved 12 Dec 2009 (online)
  54. Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7:1271–1282PubMedCrossRefGoogle Scholar
  55. Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 123:779–789PubMedCrossRefGoogle Scholar
  56. Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700PubMedCrossRefGoogle Scholar
  57. Hildmann T, Ebneth M, Pena-Cortes H, Sanchez-Serrano JJ, Willmitzer L, Prat S (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4:1157–1170PubMedCrossRefGoogle Scholar
  58. Ho CL, Saito K (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20:243–259PubMedCrossRefGoogle Scholar
  59. Hochuli M, Patzelt H, Oesterhelt D, Wuthrich K, Szyperski T (1999) Amino acid biosynthesis in the halophilic archaeon Haloarcula hispanica. J Bact 181:3226–3237PubMedGoogle Scholar
  60. Hollander-Czytko H, Grabowski J, Sandorf I, Weckermann K, Weiler EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. J Plant Phys 162:767–770CrossRefGoogle Scholar
  61. Hori H, Takabayashi K, Orvis L, Carson DA, Nobori T (1996) Gene cloning and characterization of Pseudomonas putida l-methionine-alpha-deamino-gamma-mercaptomethane-lyase. Cancer Res 56:2116–2122PubMedGoogle Scholar
  62. Imsande J (2001) Selection of soybean mutants with increased concentrations of seed methionine and cysteine. Crop Sci 41:510–515CrossRefGoogle Scholar
  63. Inoue H, Inagaki K, Sugimoto M, Esaki N, Soda K, Tanaka H (1995) Structural-analysis of the l-methionine gamma-lyase gene from Pseudomonas putida. J Biochem 117:1120–1125PubMedGoogle Scholar
  64. Jander G, Joshi V (2009) Aspartate-derived amino acid biosynthesis in Arabidopsis thaliana. In: Last RL (ed) The Arabidopsis book. The American Society of Plant Biologists, Rockville, MD, pp 1–15. doi: 10.1199/tab.0121 Google Scholar
  65. Jander G, Baerson SR, Hudak JA, Gonzalez KA, Gruys KJ, Last RL (2003) Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol 131:139–146PubMedCrossRefGoogle Scholar
  66. Jander G, Norris SR, Joshi V, Fraga M, Rugg A, Yu S, Li L, Last RL (2004) Application of a high-throughput HPLC-MS/MS assay to Arabidopsis mutant screening; evidence that threonine aldolase plays a role in seed nutritional quality. Plant J 39:465–475PubMedCrossRefGoogle Scholar
  67. Jefferson R, Goldsbrough A, Bevan M (1990) Transcriptional regulation of a patatin-1 gene in potato. Plant Mol Biol 14:995–1006PubMedCrossRefGoogle Scholar
  68. Joshi V, Jander G (2009) Arabidopsis methionine gamma-lyase is regulated according to isoleucine biosynthesis needs but plays a subordinate role to threonine deaminase. Plant Physiol 151:367–378PubMedCrossRefGoogle Scholar
  69. Joshi V, Laubengayer KM, Schauer N, Fernie AR, Jander G (2006) Two Arabidopsis threonine aldolases are nonredundant and compete with threonine deaminase for a common substrate pool. Plant Cell 18:3564–3575PubMedCrossRefGoogle Scholar
  70. Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320PubMedCrossRefGoogle Scholar
  71. Karchi H, Shaul O, Galili G (1993) Seed-specific expression of a bacterial desensitized aspartate kinase increases the production of seed threonine and methionine in transgenic tobacco. Plant J 3:721–727CrossRefGoogle Scholar
  72. Kisumi M, Komatsubara S, Chibata I (1977) Pathway for isoleucine formation from pyruvate by leucine biosynthetic-enzymes in leucine-accumulating isoleucine revertants of Serratia marcescens. J Biochem 82:95–103PubMedGoogle Scholar
  73. Kromer JO, Heinzle E, Schroder H, Wittmann C (2006) Accumulation of homolanthionine and activation of a novel pathway for isoleucine biosynthesis in Corynebacterium glutamicum McbR deletion strains. J Bact 188:609–618PubMedCrossRefGoogle Scholar
  74. Laber B, Clausen T, Huber R, Messerschmidt A, Egner U, Müller-Fahrnow A, Pohlenz H-D (1996) Cloning, purification, and crystallization of Escherichia coli cystathionine [beta]-lyase. FEBS Lett 379:94–96PubMedCrossRefGoogle Scholar
  75. Laber B, Maurer W, Hanke C, Grafe S, Ehlert S, Messerschmidt A, Clausen T (1999) Characterization of recombinant Arabidopsis thaliana threonine synthase. Eur J Biochem 263:212–221PubMedCrossRefGoogle Scholar
  76. Lea PJ, Ireland RJ (1999) Nitrogen metabolism in higher plants. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 1–47Google Scholar
  77. Lee YT, Duggleby RG (2001) Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40:6836–6844PubMedCrossRefGoogle Scholar
  78. Lee M, Leustek T (1999) Identification of the gene encoding homoserine kinase from Arabidopsis thaliana and characterization of the recombinant enzyme derived from the gene. Arch Biochem Biophys 372:135–142PubMedCrossRefGoogle Scholar
  79. Lehmann S, Funck F, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids (in press)Google Scholar
  80. Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147:316–330PubMedCrossRefGoogle Scholar
  81. Leung EWW, Guddat LW (2009) Conformational changes in a plant ketol-acid reductoisomerase upon Mg2+ and NADPH binding as revealed by two crystal structures. J Mol Biol 389:167–182PubMedCrossRefGoogle Scholar
  82. Liu XJ, Prat S, Willmitzer L, Frommer WB (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol Gen Genet 223:401–406PubMedCrossRefGoogle Scholar
  83. Lu Y, Savage LJ, Ajjawi I, Imre KM, Yoder DW, Benning C, DellaPenna D, Ohlrogge JB, Osteryoung KW, Weber AP, Wilkerson CG, Last RL (2008) New connections across pathways and cellular processes: industrialized mutant screening reveals novel associations between diverse phenotypes in Arabidopsis. Plant Physiol 146:1482–1500PubMedCrossRefGoogle Scholar
  84. Manukhov IV, Demidkina TV, Zavilgelsky GB (2005) Evolution of a gene encoding l-methionine gamma-lyase in Enterobacteriaceae family genomes. FEBS J 272:478Google Scholar
  85. Mas-Droux C, Biou V, Dumas R (2006) Allosteric threonine synthase—reorganization of the pyridoxal phosphate site upon asymmetric activation through S-adenosylmethionine binding to a novel site. J Biol Chem 281:5188–5196PubMedCrossRefGoogle Scholar
  86. McCue KF, Hanson AD (1990) Drought and salt tolerance—towards understanding and application. Trends Bact 8:358–362CrossRefGoogle Scholar
  87. McKie AE, Edlind T, Walker J, Mottram JC, Coombs GH (1998) The primitive protozoon Trichomonas vaginalis contains two methionine gamma-lyase genes that encode members of the gamma-family of pyridoxal 5′-phosphate-dependent enzymes. J Biol Chem 273:5549–5556PubMedCrossRefGoogle Scholar
  88. Mertz ET, Nelson OE, Bates LS (1964) Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145:279PubMedCrossRefGoogle Scholar
  89. Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Phys 50:1232–1248CrossRefGoogle Scholar
  90. Monticello DJ, Hadioetomo RS, Costilow RN (1984) Isoleucine synthesis by clostridium-sporogenes from propionate or alpha-methylbutyrate. J Gen Microbiol 130:309–318PubMedGoogle Scholar
  91. Mourad G, King J (1995) l-O-Methylthreonine-resistant mutant of Arabidopsis defective in isoleucine feedback-regulation. Plant Physiol 107:43–52PubMedGoogle Scholar
  92. Munck L, Karlsson KE, Hag-Berg A (1970) Gene for improved nutritional value in barley seed protein. Science 168:985–987PubMedCrossRefGoogle Scholar
  93. Nambara E, Kawaide H, Kamiya Y, Naito S (1998) Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant Cell Phys 39:853–858Google Scholar
  94. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210PubMedCrossRefGoogle Scholar
  95. Nanjo T, Fujita M, Seki M, Kato T, Tabata S, Shinozaki K (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell Phys 44:541–548CrossRefGoogle Scholar
  96. Newell-McGloughlin M (2008) Nutritionally improved agricultural crops. Plant Physiol 147:939–953PubMedCrossRefGoogle Scholar
  97. Nuccio ML, Rhodes D, McNeil SD, Hanson AD (1999) Metabolic engineering of plants for osmotic stress resistance. Curr Opin Plant Biol 2:128–134PubMedCrossRefGoogle Scholar
  98. O’Connor TR, Dyreson C, Wyrick JJ (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21:4411–4413PubMedCrossRefGoogle Scholar
  99. Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Isida J, Akiyama K, Maruyama K, Sato S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. Plant Cell Phys 44:S46–S46Google Scholar
  100. Ott KH, Kwagh JG, Stockton GW, Sidorov V, Kakefuda G (1996) Rational molecular design and genetic engineering of herbicide resistant crops by structure modeling and site-directed mutagenesis of acetohydroxyacid synthase. J Mol Biol 263:359–368PubMedCrossRefGoogle Scholar
  101. Pang SS, Guddat LW, Duggleby RG (2003) Molecular basis of sulfonylurea herbicide inhibition of acetohydroxyacid synthase. J Biol Chem 278:7639–7644PubMedCrossRefGoogle Scholar
  102. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safety 60:324–349CrossRefGoogle Scholar
  103. Phillips AT, Nuss JI, Moosic J, Foshay C (1972) Alternate pathway for isoleucine biosynthesis in Escherichia coli. J Bact 109:714–719PubMedGoogle Scholar
  104. Prell J, White JP, Bourdes A, Bunnewell S, Bongaerts RJ, Poole PS (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci USA 106:12477–12482PubMedCrossRefGoogle Scholar
  105. Rebeille F, Jabrin S, Bligny R, Loizeau K, Gambonnet B, Van Wilder V, Douce R, Ravanel S (2006) Methionine catabolism in Arabidopsis cells is initiated by a gamma-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc Natl Acad Sci USA 103:15687–15692PubMedCrossRefGoogle Scholar
  106. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher-plants. Ann Rev Plant Phys Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  107. Rhodes D, Samaras Y, D’Urzo MP, Bressan RA, Garcia-Rios MG, Csonka LN (1994) Proline accumulation during drought and salinity. J Exp Bot 45:46Google Scholar
  108. Risso C, Van Dien SJ, Orloff A, Lovley DR, Coppi MV (2008) Elucidation of an alternate isoleucine biosynthesis pathway in Geobacter sulfurreducens. J Bact 190:2266–2274PubMedCrossRefGoogle Scholar
  109. Roessner-Tunali U, Urbanczyk-Wochniak E, Czechowski T, Kolbe A, Willmitzer L, Fernie AR (2003) De novo amino acid biosynthesis in potato tubers is regulated by sucrose levels. Plant Physiol 133:683–692PubMedCrossRefGoogle Scholar
  110. Roosens N, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271PubMedCrossRefGoogle Scholar
  111. Saari L, Coterman J, Thill D (1994) Resistance to acetolactate synthase inhibiting herbicides. In: Powles S, Holtum J (eds) Herbicide resistance in plants: biology and biochemistry. Lewis Publishers, Boca Raton, pp 81–139Google Scholar
  112. Saini HS, Attieh JM, Hanson AD (1995) Biosynthesis of halomethanes and methanethiol by higher-plants via a novel methyltransferase reaction. Plant Cell Environ 18:1027–1033CrossRefGoogle Scholar
  113. Samach A, Hareven D, Gutfinger T, Ken-Dror S, Lifschitz E (1991) Biosynthetic threonine deaminase gene of tomato: isolation, structure, and upregulation in floral organs. Proc Natl Acad Sci USA 88:2678–2682PubMedCrossRefGoogle Scholar
  114. Samach A, Broday L, Hareven D, Lifschitz E (1995) Expression of an amino acid biosynthesis gene in tomato flowers: developmental upregulation and MeJa response are parenchyma-specific and mutually compatible. Plant J 8:391–406PubMedCrossRefGoogle Scholar
  115. Satoh R, Nakashima K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2002) ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis. Plant Physiol 130:709–719PubMedCrossRefGoogle Scholar
  116. Satoh R, Fujita Y, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki KY (2004) A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in Arabidopsis. Plant Cell Phys 45:309–317CrossRefGoogle Scholar
  117. Schauer N, Fernie AR (2006) Plant metabolomics: towards biological function and mechanism. Trends Plant Sci 11:508–516PubMedCrossRefGoogle Scholar
  118. Schmidt A, Rennenberg H, Wilson LG, Filner P (1985) Formation of methanethiol from methionine by leaf tissue. Phytochemistry 24:1181–1185CrossRefGoogle Scholar
  119. Schulze-Siebert D, Heineke D, Schultz G (1984) Biosynthesis of pyruvate derived amino-acids during photosynthetic carbon metabolism in spinach chloroplasts. Plant Physiol 75(Suppl 1):7Google Scholar
  120. Schuster J, Binder S (2005) The mitochondrial branched-chain aminotransferase (AtBCAT-1) is capable to initiate degradation of leucine, isoleucine and valine in almost all tissues in Arabidopsis thaliana. Plant Mol Biol 57:241–254PubMedCrossRefGoogle Scholar
  121. Shen L, Foster JG, Orcutt DM (1989) Composition and distribution of free amino-acids in flatpea (Lathyrus sylvestris L.) as influenced by water deficit and plant-age. J Exp Bot 40:71–79CrossRefGoogle Scholar
  122. Singh BK (1999) Biosynthesis of valine, leucine and isoleucine. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 227–247Google Scholar
  123. Singh R, Axtell JD (1973) A mutant gene (hl) in sorghum which improves lysine concentration in the grain. Crop Sci 13:535–539CrossRefGoogle Scholar
  124. Singh BK, Shaner DL (1995) Biosynthesis of branched chain amino acids: from test tube to field. Plant Cell 7:935–944PubMedCrossRefGoogle Scholar
  125. Singh BK, Stidham MA, Shaner DL (1988) Assay of acetohydroxyacid synthase. Anal Biochem 171:173–179PubMedCrossRefGoogle Scholar
  126. Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436PubMedCrossRefGoogle Scholar
  127. Southan MD, Copeland L (1996) Physical and kinetic properties of acetohydroxyacid synthase from wheat leaves. Physiol Plant 98:824–832CrossRefGoogle Scholar
  128. Srikrishnan M, Cotte Bvd, Montagu Mv, Verbruggen N (2002) Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiol 128:73–83CrossRefGoogle Scholar
  129. Stewart CR, Hanson AD (1980) Proline accumulation as a metabolic response to water stress. In: Kramer PJ, Turner NC (eds) Adaptation of plants to water and high temperature stress. Wiley, New York, pp 173–189Google Scholar
  130. Szamosi IT, Shaner DL, Singh BK (1994) Inhibition of threonine dehydratase is herbicidal. Plant Physiol 106:1257–1260PubMedGoogle Scholar
  131. Tan SY, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61:246–257PubMedCrossRefGoogle Scholar
  132. Taylor NL, Heazlewood JL, Day DA, Millar AH (2004) Lipoic acid-dependent oxidative catabolism of alpha-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol 134:838–848PubMedCrossRefGoogle Scholar
  133. Thoen A, Rognes S, Aarnes H (1978) Biosynthesis of threonine from homoserine in pea seedling: homoserine kinase. Plant Sci Lett 13:103–112CrossRefGoogle Scholar
  134. Thomazeau K, Curien G, Dumas R, Biou V (2001) Crystal structure of threonine synthase from Arabidopsis thaliana. Protein Sci 10:638–648PubMedCrossRefGoogle Scholar
  135. Tokoro M, Asai T, Kobayashi S, Takeuchi T, Nozaki T (2003) Identification and characterization of two isoenzymes of methionine gamma-lyase from Entamoeba histolytica—a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protist that lacks forward and reverse trans-sulfuration pathways. J Biol Chem 278:42717–42727PubMedCrossRefGoogle Scholar
  136. Tranel PJ, Wright TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700–712CrossRefGoogle Scholar
  137. Trenkamp S, Eckes P, Busch M, Fernie AR (2009) Temporally resolved GC–MS-based metabolic profiling of herbicide treated plants treated reveals that changes in polar primary metabolites alone can distinguish herbicides of differing mode of action. Metabolomics 5:277–291PubMedCrossRefGoogle Scholar
  138. Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078PubMedCrossRefGoogle Scholar
  139. Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schutze K, Alonso R, Harter K, Vicente-Carbajosa J, Droge-Laser W (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143PubMedCrossRefGoogle Scholar
  140. Wessel PM, Graciet E, Douce R, Dumas R (2000) Evidence for two distinct effector-binding sites in threonine deaminase by site-directed mutagenesis, kinetic, and binding experiments. Biochemistry 39:15136–15143PubMedCrossRefGoogle Scholar
  141. Wittenbach V, Abell L (1999) Inhibitors of valine, leucine, and isoleucine biosynthesis. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 385–416Google Scholar
  142. Wu K, Mourad G, King J (1994) A valine-resistant mutant of Arabidopsis thaliana displays an acetolactate synthase with altered feedback-control. Planta 192:249–255CrossRefGoogle Scholar
  143. Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917CrossRefGoogle Scholar
  144. Wu B, Zhang B, Feng X, Rubens JR, Huang R, Hicks LM, Pakrasi HB, Tang YJ (2009) Alternate isoleucine synthesis pathway in cyanobacterial species. Microbiology. Epub ahead of print. doi: 10.1099/mic.0.031799-0
  145. Xu H, Zhang YZ, Guo XK, Ren SX, Staempfli AA, Chiao JS, Jiang WH, Zhao GP (2004) Isoleucine biosynthesis in Leptospira interrogans serotype lai strain 56601 proceeds via a threonine-independent pathway. J Bact 186:5400–5409PubMedCrossRefGoogle Scholar
  146. Yoshizawa F (2004) Regulation of protein synthesis by branched-chain amino acids in vivo. Biochem Biophys Res Commun 313:417–422PubMedCrossRefGoogle Scholar
  147. Zeh M, Casazza AP, Kreft O, Roessner U, Bieberich K, Willmitzer L, Hoefgen R, Hesse H (2001) Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol 127:792–802PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Vijay Joshi
    • 1
  • Je-Gun Joung
    • 1
  • Zhangjun Fei
    • 1
    • 2
  • Georg Jander
    • 1
  1. 1.Boyce Thompson Institute for Plant ResearchIthacaUSA
  2. 2.United States Department of Agriculture-Agricultural Research ServiceRobert W. Holley Center for Agriculture and HealthIthacaUSA

Personalised recommendations