1932
0

Annual Review of Plant Biology

Volume 67, 2016

The Regulation of Essential Amino Acid Synthesis and Accumulation in Plants

Abstract

Although amino acids are critical for all forms of life, only proteogenic amino acids that humans and animals cannot synthesize de novo and therefore must acquire in their diets are classified as essential. Nine amino acids—lysine, methionine, threonine, phenylalanine, tryptophan, valine, isoleucine, leucine, and histidine—fit this definition. Despite their nutritional importance, several of these amino acids are present in limiting quantities in many of the world's major crops. In recent years, a combination of reverse genetic and biochemical approaches has been used to define the genes encoding the enzymes responsible for synthesizing, degrading, and regulating these amino acids. In this review, we describe recent advances in our understanding of the metabolism of the essential amino acids, discuss approaches for enhancing their levels in plants, and appraise efforts toward their biofortification in crop plants.

Keyword(s): cellular energy, metabolism, nutrition
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043015-112213
2016-04-29
2025-06-22
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043015-112213.html?itemId=/content/journals/10.1146/annurev-arplant-043015-112213&mimeType=html&fmt=ahah

Literature Cited

  1. Alban C, Baldet P, Axiotis S, Douce R. 1.  1993. Purification and characterization of 3-methylcrotonyl-coenzyme-A carboxylase from higher-plant mitochondria. Plant Physiol. 102:957–65 [Google Scholar]
  2. Alseekh S, Tohge T, Wendenberg R, Scossa F, Omranian N. 2.  et al. 2015. Identification and mode of inheritance of quantitative trait loci for secondary metabolite abundance in tomato. Plant Cell 27:485–512 [Google Scholar]
  3. Ames BN, Garry B, Herzenberg LA. 3.  1960. The genetic control of the enzymes of histidine biosynthesis in Salmonella typhimurium. J. Gen. Microbiol. 22:369–78 [Google Scholar]
  4. Amir R. 4.  2010. Current understanding of the factors regulating methionine content in vegetative tissues of higher plants. Amino Acids 39:917–31 [Google Scholar]
  5. Amir R, Hacham Y, Galili G. 5.  2002. Cystathionine γ-synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends Plant Sci. 7:153–56 [Google Scholar]
  6. Angelovici R, Fait A, Fernie AR, Galili G. 6.  2011. A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol. 189:148–59 [Google Scholar]
  7. Angelovici R, Fait A, Zhu X, Szymanski J, Feldmesser E. 7.  et al. 2009. Deciphering transcriptional and metabolic networks associated with lysine metabolism during Arabidopsis seed development. Plant Physiol. 151:2058–72 [Google Scholar]
  8. Angelovici R, Lipka AE, Deason N, Gonzalez-Jorge S, Lin H. 8.  et al. 2013. Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25:4827–43Describes the first genome-wide association study of plant amino acid levels. [Google Scholar]
  9. Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T. 9.  et al. 2010. Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22:1549–63 [Google Scholar]
  10. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. 10.  2011. Protein degradation—an alternative respiratory substrate for stressed plants. Trends Plant Sci. 16:489–98Summarizes data showing that in plants, amino acids are not only used for protein synthesis but also serve as energy donors via their degradation in the TCA cycle. [Google Scholar]
  11. Atkinson NJ, Lilley CJ, Urwin PE. 11.  2013. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 162:2028–41 [Google Scholar]
  12. Avin-Wittenberg T, Bajdzienko K, Wittenberg G, Alseekh S, Tohge T. 12.  et al. 2015. Global analysis of the role of autophagy in cellular metabolism and energy homeostasis in Arabidopsis seedlings under carbon starvation. Plant Cell 27:306–22Shows that autophagy serves as an essential process, helping organisms mobilize proteins as an energy source and thus survive when they are starved of various important metabolites (particularly carbohydrates). [Google Scholar]
  13. Avraham T, Amir R. 13.  2005. The expression level of threonine synthase and cystathionine-γ-synthase is influenced by the level of both threonine and methionine in Arabidopsis plants. Transgenic Res. 14:299–311 [Google Scholar]
  14. Avraham T, Badani H, Galili S, Amir R. 14.  2005. Enhanced levels of methionine and cysteine in transgenic alfalfa (Medicago sativa L.) plants over-expressing the Arabidopsis cystathionine γ-synthase gene. Plant Biotechnol. J. 3:71–79 [Google Scholar]
  15. Azevedo RA, Arruda P. 15.  2010. High-lysine maize: the key discoveries that have made it possible. Amino Acids 39:979–89Describes attempts to enhance accumulation of Lys, one of the most critical essential amino acids in the human diet. [Google Scholar]
  16. Azevedo RA, Arruda P, Turner WL, Lea PJ. 16.  1997. The biosynthesis and metabolism of the aspartate derived amino acids in higher plants. Phytochemistry 46:395–419 [Google Scholar]
  17. Bartlem D, Lambein I, Okamoto T, Itaya A, Uda Y. 17.  et al. 2000. Mutation in the threonine synthase gene results in an over-accumulation of soluble methionine in Arabidopsis. Plant Physiol. 123:101–10 [Google Scholar]
  18. Basset GJC, Quinlivan EP, Ravanel S, Rebeille F, Nichols BP. 18.  et al. 2004. Foliate synthesis in plants: The p-aminobenzoate branch is initiated by a bifunctional PabA-PabB protein that is targeted to plastids. PNAS 101:1496–501 [Google Scholar]
  19. Ben-Tzvi Tzchori I, Perl A, Galili G. 19.  1996. Lysine and threonine metabolism are subject to complex patterns of regulation in Arabidopsis. Plant Mol. Biol. 32:727–34 [Google Scholar]
  20. Binder S. 20.  2010. Branched-chain amino acid metabolism in Arabidopsis thaliana. Arabidopsis Book 8:e0137 [Google Scholar]
  21. Biou V, Dumas R, Cohen-Addad C, Douce R, Job D, Pebay-Peyroula E. 21.  1997. The crystal structure of plant acetohydroxy acid isomeroreductase complexed with NADPH, two magnesium ions and a herbicidal transition state analog determined at 1.65 Å resolution. EMBO J. 16:3405–15 [Google Scholar]
  22. Boerjan W, Bauw G, Vanmontagu M, Inze D. 22.  1994. Distinct phenotypes generated by overexpression and suppression of S-adenosyl-l-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6:1401–14 [Google Scholar]
  23. Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC. 23.  et al. 1999. S-methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11:1485–97 [Google Scholar]
  24. Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P. 24.  et al. 2012. Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Mol. Plant 5:418–29 [Google Scholar]
  25. Brinch-Pedersen H, Galili G, Knudsen S, Holm PB. 25.  1996. Engineering of the aspartate family biosynthetic pathway in barley (Hordeum vulgare L.) by transformation with heterologous genes encoding feed-back-insensitive aspartate kinase and dihydrodipicolinate synthase. Plant Mol. Biol. 32:611–20 [Google Scholar]
  26. Bunsupa S, Katayama K, Ikeura E, Oikawa A, Toyooka K. 26.  et al. 2012. Lysine decarboxylase catalyzes the first step of quinolizidine alkaloid biosynthesis and coevolved with alkaloid production in Leguminosae. Plant Cell 24:1202–16Describes the role of Lys as a precursor for various components important for plant environmental responses. [Google Scholar]
  27. Byeon Y, Park S, Lee HY, Kim Y-S, Back K. 27.  2014. Elevated production of melatonin in transgenic rice seeds expressing rice tryptophan decarboxylase. J. Pineal Res. 56:275–82 [Google Scholar]
  28. Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R. 28.  et al. 2011. High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant J. 67:869–84 [Google Scholar]
  29. Campbell MA, Patel JK, Meyers JL, Myrick LC, Gustin JL. 29.  2001. Genes encoding for branched-chain amino acid aminotransferase are differentially expressed in plants. Plant Physiol. Biochem. 39:855–60 [Google Scholar]
  30. Chen W, Taylor NL, Chi Y, Millar AH, Lambers H, Finnegan PM. 30.  2014. The metabolic acclimation of Arabidopsis thaliana to arsenate is sensitized by the loss of mitochondrial LIPOAMIDE DEHYDROGENASE2, a key enzyme in oxidative metabolism. Plant Cell Environ. 37:684–95 [Google Scholar]
  31. Chiaiese P, Ohkama-Ohtsu N, Molvig L, Godfree R, Dove H. 31.  et al. 2004. Sulphur and nitrogen nutrition influence the response of chickpea seeds to an added, transgenic sink for organic sulphur. J. Exp. Bot. 55:1889–901 [Google Scholar]
  32. Chiba Y, Sakurai R, Yoshino M, Ominato K, Ishikawa M. 32.  et al. 2003. S-adenosyl-l-methionine is an effector in the posttranscriptional autoregulation of the cystathionine γ-synthase gene in Arabidopsis. PNAS 100:10225–30 [Google Scholar]
  33. Cohen H, Israeli H, Matityahu I, Amir R. 33.  2014. Seed-specific expression of a feedback-insensitive form of CYSTATHIONINE γ-SYNTHASE in Arabidopsis stimulates metabolic and transcriptomic responses associated with desiccation stress. Plant Physiol. 166:1575–92 [Google Scholar]
  34. Curien G, Bastlen O, Robert-Genthon M, Cornish-Bowden A, Cardenas ML, Dumas R. 34.  2009. Understanding the regulation of aspartate metabolism using a model based on measured kinetic parameters. Mol. Syst. Biol. 5:271Uses computational modeling to provide considerable insight into the complex networks of amino acid metabolism. [Google Scholar]
  35. Curien G, Biou V, Mas-Droux C, Robert-Genthon M, Ferrer J-L, Dumas R. 35.  2008. Amino acid biosynthesis: new architectures in allosteric enzymes. Plant Physiol. Biochem. 46:325–39 [Google Scholar]
  36. Curien G, Job D, Douce R, Dumas R. 36.  1998. Allosteric activation of Arabidopsis threonine synthase by S-adenosylmethionine. Biochemistry 37:13212–21 [Google Scholar]
  37. Dal Cin V, Tieman DM, Tohge T, McQuinn R, de Vos RCH. 37.  et al. 2011. Identification of genes in the phenylalanine metabolic pathway by ectopic expression of a MYB transcription factor in tomato fruit. Plant Cell 23:2738–53 [Google Scholar]
  38. Daschner K, Couee I, Binder S. 38.  2001. The mitochondrial isovaleryl-coenzyme A dehydrogenase of Arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol. 126:601–12 [Google Scholar]
  39. Daschner K, Thalheim C, Guha C, Brennicke A, Binder S. 39.  1999. In plants a putative isovaleryl-CoA-dehydrogenase is located in mitochondria. Plant Mol. Biol. 39:1275–82 [Google Scholar]
  40. de Kraker J-W, Luck K, Textor S, Tokuhisa JG, Gershenzon J. 40.  2007. Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine. Plant Physiol. 143:970–86 [Google Scholar]
  41. Di R, Kim J, Martin MN, Leustek T, Jhoo JW. 41.  et al. 2003. Enhancement of the primary flavor compound methional in potato by increasing the level of soluble methionine. J. Agric. Food Chem. 51:5695–702 [Google Scholar]
  42. Diebold R, Schuster J, Daschner K, Binder S. 42.  2002. The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol. 129:540–50 [Google Scholar]
  43. Ding G, Che P, Ilarslan H, Wurtele ES, Nikolau BJ. 43.  2012. Genetic dissection of methylcrotonyl CoA carboxylase indicates a complex role for mitochondrial leucine catabolism during seed development and germination. Plant J. 70:562–77 [Google Scholar]
  44. Dixon RA, Harrison MJ, Lamb CJ. 44.  1994. Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32:479–501 [Google Scholar]
  45. Dubouzet JG, Ishihara A, Matsuda F, Miyagawa H, Iwata H, Wakasa K. 45.  2007. Integrated metabolomic and transcriptomic analyses of high-tryptophan rice expressing a mutant anthranilate synthase alpha subunit. J. Exp. Bot. 58:3309–21 [Google Scholar]
  46. Duggleby RG, McCourt JA, Guddat LW. 46.  2008. Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol. Biochem. 46:309–24 [Google Scholar]
  47. Dumas R, Biou V, Halgand F, Douce R, Duggleby RG. 47.  2001. Enzymology, structure, and dynamics of acetohydroxy acid isomeroreductase. Acc. Chem. Res. 34:399–408 [Google Scholar]
  48. Ebisuno T, Shigesada K, Katsuki H. 48.  1975. d-α-Hydroxyglutarate dehydrogenase of Rhodospirillum rubrum. J. Biochem. 78:1321–29 [Google Scholar]
  49. Elango R, Ball RO, Pencharz PB. 49.  2009. Amino acid requirements in humans: with a special emphasis on the metabolic availability of amino acids. Amino Acids 37:19–27 [Google Scholar]
  50. Engqvist M, Drincovich MF, Fluegge U-I, Maurino VG. 50.  2009. Two d-2-hydroxy-acid dehydrogenases in Arabidopsis thaliana with catalytic capacities to participate in the last reactions of the methylglyoxal and β-oxidation pathways. J. Biol. Chem. 284:25026–37 [Google Scholar]
  51. Eubel H, Meyer EH, Taylor NL, Bussell JD, O'Toole N. 51.  et al. 2008. Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148:1809–29 [Google Scholar]
  52. Faivre-Nitschke SE, Couee I, Vermel M, Grienenberger JM, Gualberto JM. 52.  2001. Purification, characterization and cloning of isovaleryl-CoA dehydrogenase from higher plant mitochondria. Eur. J. Biochem. 268:1332–39 [Google Scholar]
  53. Falco SC, Guida T, Locke M, Mauvais J, Sanders C. 53.  et al. 1995. Transgenic canola and soybean seeds with increased lysine. Biotechnology 13:577–82 [Google Scholar]
  54. Field B, Cardon G, Traka M, Botterman J, Vancanneyt G, Mithen R. 54.  2004. Glucosinolate and amino acid biosynthesis in Arabidopsis. Plant Physiol. 135:828–39 [Google Scholar]
  55. Frank A, Cohen H, Hoffman D, Amir R. 55.  2015. Methionine and S-methylmethionine exhibit temporal and spatial accumulation patterns during the Arabidopsis life cycle. Amino Acids 47:497–510 [Google Scholar]
  56. Frankard V, Ghislain M, Negrutiu I, Jacobs M. 56.  1991. High threonine producer mutant of Nicotiana sylvestris (Spegg. and Comes). Theor. Appl. Genet. 82:273–82 [Google Scholar]
  57. Frizzi A, Huang S, Gilbertson LA, Armstrong TA, Luethy MH, Malvar TM. 57.  2008. Modifying lysine biosynthesis and catabolism in corn with a single bifunctional expression/silencing transgene cassette. Plant Biotechnol. J. 6:13–21 [Google Scholar]
  58. Fürst PPS. 58.  2004. What are the essential elements needed for the determination of amino acid requirements in humans?. J. Nutr. 134:1558S–65S [Google Scholar]
  59. Galili G. 59.  2002. New insights into the regulation and functional significance of lysine metabolism in plants. Annu. Rev. Plant Biol. 53:27–43 [Google Scholar]
  60. Galili G, Amir R. 60.  2013. Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality. Plant Biotechnol. J. 11:211–22Reviews biofortification of the essential amino acids Lys and Met. [Google Scholar]
  61. Galili G, Amir R, Hoefgen R, Hesse H. 61.  2005. Improving the levels of essential amino acids and sulfur metabolites in plants. Biol. Chem. 386:817–31 [Google Scholar]
  62. Galili G, Tang GL, Zhu XH, Karchi H, Miron D. 62.  et al. 2001. Molecular genetic dissection and potential manipulation of lysine metabolism in seeds. J. Plant Physiol. 158:515–20 [Google Scholar]
  63. Gallardo K, Firnhaber C, Zuber H, Hericher D, Belghazi M. 63.  et al. 2007. A combined proteome and transcriptome analysis of developing Medicago truncatula seeds. Mol. Cell. Proteom. 6:2165–79 [Google Scholar]
  64. Gao F, Wang C, Wei C, Li Y. 64.  2009. A branched-chain aminotransferase may regulate hormone levels by affecting KNOX genes in plants. Planta 230:611–23 [Google Scholar]
  65. Garcion C, Lohmann A, Lamodiere E, Catinot J, Buchala A. 65.  et al. 2008. Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol. 147:1279–87 [Google Scholar]
  66. Geigenberger P, Fernie AR. 66.  2014. Metabolic control of redox and redox control of metabolism in plants. Antioxid. Redox Signal. 21:1389–421 [Google Scholar]
  67. Giri R, Sureshkumar MS, Naskar K, Bharadwaj YK, Sarma KSS. 67.  et al. 2008. Electron beam irradiation of LLDPE and PDMS rubber blends: studies on the physicomechanical properties. Adv. Polym. Technol. 27:98–107 [Google Scholar]
  68. Gonda I, Bar E, Portnoy V, Lev S, Burger J. 68.  et al. 2010. Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. fruit. J. Exp. Bot. 61:1111–23 [Google Scholar]
  69. Gonda I, Lev S, Bar E, Sikron N, Portnoy V. 69.  et al. 2013. Catabolism of l-methionine in the formation of sulfur and other volatiles in melon (Cucumis melo L.) fruit. Plant J. 74:458–72Describes the role of amino acids as precursors of volatile compounds, some of which contribute to the flavor and aroma of fruits and vegetables. [Google Scholar]
  70. Goto DB, Ogi M, Kijima F, Kumagai T, van Werven F. 70.  et al. 2002. A single-nucleotide mutation in a gene encoding S-adenosylmethionine synthetase is associated with methionine over-accumulation phenotype in Arabidopsis thaliana. Genes Genet. Syst. 77:89–95 [Google Scholar]
  71. Goyer A, Collakova E, Shachar-Hill Y, Hanson AD. 71.  2007. Functional characterization of a methionine γ-lyase in Arabidopsis and its implication in an alternative to the reverse trans-sulfuration pathway. Plant Cell Physiol. 48:232–42 [Google Scholar]
  72. Graindorge M, Giustini C, Jacomin AC, Kraut A, Curien G, Matringe M. 72.  2010. Identification of a plant gene encoding glutamate/aspartate-prephenate aminotransferase: the last homeless enzyme of aromatic amino acids biosynthesis. FEBS Lett. 584:4357–60 [Google Scholar]
  73. Gu L, Jones AD, Last RL. 73.  2010. Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J. 61:579–90Shows that amino acid catabolism mutants are unable to degrade amino acids to be used as energy sources, and hence that mutant organisms lacking amino acid catabolism are generally fitness impaired. [Google Scholar]
  74. Hacham Y, Avraham T, Amir R. 74.  2002. The N-terminal region of Arabidopsis cystathionine γ-synthase plays an important regulatory role in methionine metabolism. Plant Physiol. 128:454–62 [Google Scholar]
  75. Hacham Y, Matityahu I, Amir R. 75.  2013. Light and sucrose up-regulate the expression level of Arabidopsis cystathionine γ-synthase, the key enzyme of methionine biosynthesis pathway. Amino Acids 45:1179–90 [Google Scholar]
  76. Hacham Y, Matityahu I, Schuster G, Amir R. 76.  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. 54:260–71 [Google Scholar]
  77. Hacham Y, Schuster G, Amir R. 77.  2006. An in vivo internal deletion in the N-terminus region of Arabidopsis cystathionine γ-synthase results in CGS expression that is insensitive to methionine. Plant J. 45:955–67 [Google Scholar]
  78. Hagelstein P, Schultz G. 78.  1993. Leucine synthesis in spinach chloroplasts alpha-isopropylmalate synthase (EC 4.1.3.12). Biol. Chem. Hoppe Seyler 374:767–68 [Google Scholar]
  79. Hagelstein P, Sieve B, Klein M, Jans H, Schultz G. 79.  1997. Leucine synthesis in chloroplasts: Leucine/isoleucine aminotransferase and valine aminotransferase are different enzymes in spinach chloroplasts. J. Plant Physiol. 150:23–30 [Google Scholar]
  80. Halgand F, Wessel PM, Laprevote O, Dumas R. 80.  2002. Biochemical and mass spectrometric evidence for quaternary structure modifications of plant threonine deaminase induced by isoleucine. Biochemistry 41:13767–73 [Google Scholar]
  81. Harding MM. 81.  2004. The architecture of metal coordination groups in proteins. Acta Crystallogr. D 60:849–59 [Google Scholar]
  82. He Y, Mawhinney TP, Preuss ML, Schroeder AC, Chen B. 82.  et al. 2009. A redox-active isopropylmalate dehydrogenase functions in the biosynthesis of glucosinolates and leucine in Arabidopsis. Plant J. 60:679–90 [Google Scholar]
  83. He YK, Li JY. 83.  2001. Differential expression of triplicate phosphoribosylanthranilate isomerase isogenes in the tryptophan biosynthetic pathway of Arabidopsis thaliana (L.) Heynh. Planta 212:641–47 [Google Scholar]
  84. Heilskov S, Rytter MJH, Vestergaard C, Briend A, Babirekere E, Deleuran MS. 84.  2014. Dermatosis in children with oedematous malnutrition (Kwashiorkor): a review of the literature. J. Eur. Acad. Dermatol. Venereol. 28:995–1001 [Google Scholar]
  85. Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T. 85.  et al. 2007. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. PNAS 104:6478–83 [Google Scholar]
  86. Hournard NM, Mainville JL, Bonin CP, Huang S, Luethy MH, Malvar TM. 86.  2007. High-lysine corn generated by endosperm-specific suppression of lysine catabolism using RNAi. Plant Biotechnol. J. 5:605–14 [Google Scholar]
  87. Huang TF, Tohge T, Lytovchenko A, Fernie AR, Jander G. 87.  2010. Pleiotropic physiological consequences of feedback-insensitive phenylalanine biosynthesis in Arabidopsis thaliana. Plant J. 63:823–35 [Google Scholar]
  88. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY. 88.  2004. Expression of a feedback-resistant anthranilate synthase in Catharanthus roseus hairy roots provides evidence for tight regulation of terpenoid indole alkaloid levels. Biotechnol. Bioeng. 86:718–27 [Google Scholar]
  89. Imsande J. 89.  2001. Selection of soybean mutants with increased concentrations of seed methionine and cysteine. Crop Sci. 41:510–15 [Google Scholar]
  90. Ingle RA. 90.  2011. Histidine biosynthesis. Arabidopsis Book 9:e0141 [Google Scholar]
  91. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ. 91.  2005. The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17:2587–600 [Google Scholar]
  92. Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ. 92.  2006. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J. 47:751–60 [Google Scholar]
  93. Jander G, Joshi V. 93.  2009. Aspartate-derived amino acid biosynthesis in Arabidopsis thaliana. Arabidopsis Book 7:e0121 [Google Scholar]
  94. Jander G, Joshi V. 94.  2010. Recent progress in deciphering the biosynthesis of aspartate-derived amino acids in plants. Mol. Plant 3:54–65 [Google Scholar]
  95. Jander G, Norris SR, Joshi V, Fraga M, Rugg A. 95.  et al. 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. 39:465–75 [Google Scholar]
  96. Joshi V, Jander G. 96.  2009. Arabidopsis methionine γ-lyase is regulated according to isoleucine biosynthesis needs but plays a subordinate role to threonine deaminase. Plant Physiol. 151:367–78 [Google Scholar]
  97. Joshi V, Joung J-G, Fei Z, Jander G. 97.  2010. Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–47 [Google Scholar]
  98. Joshi V, Laubengayer KM, Schauer N, Fernie AR, Jander G. 98.  2006. Two Arabidopsis threonine aldolases are nonredundant and compete with threonine deaminase for a common substrate pool. Plant Cell 18:3564–75 [Google Scholar]
  99. Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G. 99.  et al. 2006. Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J. Biol. Chem. 281:23357–66 [Google Scholar]
  100. Karchi H, Shaul O, Galili G. 100.  1993. Seed-specific expression of a bacterial desensitized aspartate kinase increases the production of seed threonine and methionine in transgenic tobacco. Plant J. 3:721–27 [Google Scholar]
  101. Karchi H, Shaul O, Galili G. 101.  1994. Lysine synthesis and catabolism are coordinately regulated during tobacco seed development. PNAS 91:2577–81 [Google Scholar]
  102. Katz YS, Galili G, Amir R. 102.  2006. Regulatory role of cystathionine-γ-synthase and de novo synthesis of methionine in ethylene production during tomato fruit ripening. Plant Mol. Biol. 61:255–68 [Google Scholar]
  103. Kim J, Lee M, Chalam R, Martin MN, Leustek T, Boerjan W. 103.  2002. Constitutive overexpression of cystathionine γ-synthase in Arabidopsis leads to accumulation of soluble methionine and S-methylmethionine. Plant Physiol. 128:95–107 [Google Scholar]
  104. Kim W-S, Jez JM, Krishnan HB. 104.  2014. Effects of proteome rebalancing and sulfur nutrition on the accumulation of methionine rich δ-zein in transgenic soybeans. Front. Plant Sci. 5:633 [Google Scholar]
  105. Kirma M, Araujo WL, Fernie AR, Galili G. 105.  2012. The multifaceted role of aspartate-family amino acids in plant metabolism. J. Exp. Bot. 63:4995–5001 [Google Scholar]
  106. Knill T, Reichelt M, Paetz C, Gershenzon J, Binder S. 106.  2009. Arabidopsis thaliana encodes a bacterial-type heterodimeric isopropylmalate isomerase involved in both Leu biosynthesis and the Met chain elongation pathway of glucosinolate formation. Plant Mol. Biol. 71:227–39 [Google Scholar]
  107. Knill T, Schuster J, Reichelt M, Gershenzon J, Binder S. 107.  2008. Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol. 146:1028–39 [Google Scholar]
  108. Kochevenko A, Araujo WL, Maloney GS, Tieman DM, Do PT. 108.  et al. 2012. Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Mol. Plant 5:366–75 [Google Scholar]
  109. Kochevenko A, Fernie AR. 109.  2011. The genetic architecture of branched-chain amino acid accumulation in tomato fruits. J. Exp. Bot. 62:3895–906 [Google Scholar]
  110. Kramer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC. 110.  1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–38 [Google Scholar]
  111. Krishnan HB. 111.  2005. Engineering soybean for enhanced sulfur amino acid content. Crop Sci. 45:454–61 [Google Scholar]
  112. Kroymann J, Textor S, Tokuhisa JG, Falk KL, Bartram S. 112.  et al. 2001. A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol. 127:1077–88 [Google Scholar]
  113. Kusano M, Tohge T, Fukushima A, Kobayashi M, Hayashi N. 113.  et al. 2011. Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. Plant J. 67:354–69 [Google Scholar]
  114. Lächler K, Imhof J, Reichelt M, Gershenzon J, Binder S. 114.  2015. The cytosolic branched-chain aminotransferases of Arabidopsis thaliana influence methionine supply, salvage and glucosinolate metabolism. Plant Mol. Biol. 88:119–31 [Google Scholar]
  115. Lee M, Martin MN, Hudson AO, Lee J, Muhitch MJ, Leustek T. 115.  2005. Methionine and threonine synthesis are limited by homoserine availability and not the activity of homoserine kinase in Arabidopsis thaliana. Plant J. 41:685–96 [Google Scholar]
  116. Lee MS, Huang TF, Toro-Ramos T, Fraga M, Last RL, Jander G. 116.  2008. Reduced activity of Arabidopsis thaliana HMT2, a methionine biosynthetic enzyme, increases seed methionine content. Plant J. 54:310–20 [Google Scholar]
  117. Lee YT, Duggleby RG. 117.  2001. Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40:6836–44 [Google Scholar]
  118. Less H, Angelovici R, Tzin V, Galili G. 118.  2011. Coordinated gene networks regulating Arabidopsis plant metabolism in response to various stresses and nutritional cues. Plant Cell 23:1264–71 [Google Scholar]
  119. Less H, Galili G. 119.  2008. Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 147:316–30 [Google Scholar]
  120. Less H, Galili G. 120.  2009. Coordinations between gene modules control the operation of plant amino acid metabolic networks. BMC Syst. Biol. 3:14 [Google Scholar]
  121. Leung EWW, Guddat LW. 121.  2009. Conformational changes in a plant ketol-acid reductoisomerase upon Mg2+ and NADPH binding as revealed by two crystal structures. J. Mol. Biol. 389:167–82 [Google Scholar]
  122. Li J, Last RL. 122.  1996. The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol. 110:51–59 [Google Scholar]
  123. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR. 123.  2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1:387–96 [Google Scholar]
  124. Lisec J, Steinfath M, Meyer RC, Selbig J, Melchinger AE. 124.  et al. 2009. Identification of heterotic metabolite QTL in Arabidopsis thaliana RIL and IL populations. Plant J. 59:777–88 [Google Scholar]
  125. Maeda H, Dudareva N. 125.  2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol. 63:73–105 [Google Scholar]
  126. Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G. 126.  et al. 2010. RNAi suppression of Arogenate Dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals. Plant Cell 22:832–49 [Google Scholar]
  127. Maeda H, Yoo H, Dudareva N. 127.  2011. Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate. Nat. Chem. Biol. 7:19–21 [Google Scholar]
  128. Maimann S, Hoefgen R, Hesse H. 128.  2001. Enhanced cystathionine beta-lyase activity in transgenic potato plants does not force metabolite flow towards methionine. Planta 214:163–70 [Google Scholar]
  129. Malatrasi M, Corradi M, Svensson JT, Close TJ, Gulli M, Marmiroli N. 129.  2006. A branched-chain amino acid aminotransferase gene isolated from Hordeum vulgare is differentially regulated by drought stress. Theor. Appl. Genet. 113:965–76 [Google Scholar]
  130. Maloney GS, Kochevenko A, Tieman DM, Tohge T, Krieger U. 130.  et al. 2010. Characterization of the branched-chain amino acid aminotransferase enzyme family in tomato. Plant Physiol. 153:925–36 [Google Scholar]
  131. Mas-Droux C, Curien G, Robert-Genthon M, Laurencin M, Ferrer J-L, Dumas R. 131.  2006. A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis aspartate kinase. Plant Cell 18:1681–92 [Google Scholar]
  132. Matityahu I, Godo I, Hacham Y, Amir R. 132.  2013. Tobacco seeds expressing feedback-insensitive cystathionine gamma-synthase exhibit elevated content of methionine and altered primary metabolic profile. BMC Plant Biol. 13:206 [Google Scholar]
  133. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E. 133.  et al. 2008. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 49:1135–49 [Google Scholar]
  134. McCourt JA, Pang SS, King-Scott J, Guddat LW, Duggleby RG. 134.  2006. Herbicide-binding sites revealed in the structure of plant acetohydroxyacid synthase. PNAS 103:569–73 [Google Scholar]
  135. Meinke D, Muralla R, Sweeney C, Dickerman A. 135.  2008. Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci. 13:483–91 [Google Scholar]
  136. Mertz ET, Nelson OE, Bates LS. 136.  1964. Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145:279–80 [Google Scholar]
  137. Miles EW. 137.  2001. Tryptophan synthase: a multienzyme complex with an intramolecular tunnel. Chem. Rec. 1:140–51 [Google Scholar]
  138. Millar AH, Sweetlove LJ, Giege P, Leaver CJ. 138.  2001. Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127:1711–27 [Google Scholar]
  139. Mills PB, Struys E, Jakobs C, Plecko B, Baxter P. 139.  et al. 2006. Mutations in antiquitin in individuals with pyridoxine-dependent seizures. Nat. Med. 12:307–9 [Google Scholar]
  140. Mooney BP, Miernyk JA, Randall DD. 140.  2002. The complex fate of α-ketoacids. Annu. Rev. Plant Biol. 53:357–75 [Google Scholar]
  141. Mori I, Fonnepfister R, Matsunaga S, Tada S, Kimura Y. 141.  et al. 1995. A novel class of herbicides—specific inhibitors of imidazoleglycerol phosphate dehydratase. Plant Physiol. 107:719–23 [Google Scholar]
  142. Mourad G, King J. 142.  1995. l-O-Methylthreonine-resistant mutant of Arabidopsis defective in isoleucine feedback regulation. Plant Physiol. 107:43–52 [Google Scholar]
  143. Muralla R, Sweeney C, Stepansky A, Leustek T, Meinke D. 143.  2007. Genetic dissection of histidine biosynthesis in Arabidopsis. Plant Physiol. 144:890–903 [Google Scholar]
  144. Negrutiu I, Cattoirreynearts A, Verbruggen I, Jacobs M. 144.  1984. Lysine overproducer mutants with an altered dihydrodipicolinate synthase from protoplast culture of Nicotiana sylvestris (Spegazzini and Comes). Theor. Appl. Genet. 68:11–20 [Google Scholar]
  145. Nikiforova V, Kempa S, Zeh M, Maimann S, Kreft O. 145.  et al. 2002. Engineering of cysteine and methionine biosynthesis in potato. Amino Acids 22:259–78 [Google Scholar]
  146. Niyogi KK, Last RL, Fink GR, Keith B. 146.  1993. Suppressors of trp1 fluorescence identify a new Arabidopsis gene, TRP4, encoding the anthranilate synthase β subunit. Plant Cell 5:1011–27 [Google Scholar]
  147. Noctor G, Novitskaya L, Lea PJ, Foyer CH. 147.  2002. Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation. J. Exp. Bot. 53:939–45 [Google Scholar]
  148. Obata T, Fernie AR. 148.  2012. The use of metabolomics to dissect plant responses to abiotic stresses. Cell. Mol. Life Sci. 69:3225–43 [Google Scholar]
  149. Obata T, Matthes A, Koszior S, Lehmann M, Araujo WL. 149.  et al. 2011. Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 72:1081–91 [Google Scholar]
  150. Ohta D, Fujimori K, Mizutani M, Nakayama Y, Kunpaisal-Hashimoto R. 150.  et al. 2000. Molecular cloning and characterization of ATP-phosphoribosyl transferase from Arabidopsis, a key enzyme in the histidine biosynthetic pathway. Plant Physiol. 122:907–14 [Google Scholar]
  151. Oliva M, Ovadia R, Perl A, Bar E, Lewinsohn E. 151.  et al. 2015. Enhanced formation of aromatic amino acids increases fragrance without affecting flower longevity or pigmentation in Petunia × hybrida. Plant Biotechnol. J. 13:125–36 [Google Scholar]
  152. Onouchi H, Lambein I, Sakurai R, Suzuki A, Chiba Y, Naito S. 152.  2004. Autoregulation of the gene for cystathionine γ-synthase in Arabidopsis: post-transcriptional regulation induced by S-adenosylmethionine. Biochem. Soc. Trans. 32:597–600 [Google Scholar]
  153. Onouchi H, Nagami Y, Haraguchi Y, Nakamoto M, Nishimura Y. 153.  et al. 2005. Nascent peptide-mediated translation elongation arrest coupled with mRNA degradation in the CGS1 gene of Arabidopsis. Genes Dev. 19:1799–810 [Google Scholar]
  154. Perl A, Shaul O, Galili G. 154.  1992. Regulation of lysine synthesis in transgenic potato plants expressing a bacterial dihydrodipicolinate synthase in their chloroplasts. Plant Mol. Biol. 19:815–23 [Google Scholar]
  155. Petersen LN, Marineo S, Mandala S, Davids F, Sewell BT, Ingle RA. 155.  2010. The missing link in plant histidine biosynthesis: Arabidopsis myoinositol monophosphatase-like2 encodes a functional histidinol-phosphate phosphatase. Plant Physiol. 152:1186–96 [Google Scholar]
  156. Pratelli R, Pilot G. 156.  2014. Regulation of amino acid metabolic enzymes and transporters in plants. J. Exp. Bot. 65:5535–56 [Google Scholar]
  157. Ranocha P, McNeil SD, Ziemak MJ, Li CJ, Tarczynski MC, Hanson AD. 157.  2001. The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity. Plant J. 25:575–84 [Google Scholar]
  158. Ravanel S, Gakiere B, Job D, Douce R. 158.  1998. The specific features of methionine biosynthesis and metabolism in plants. PNAS 95:7805–12 [Google Scholar]
  159. Rees JD, Ingle RA, Smith JAC. 159.  2009. Relative contributions of nine genes in the pathway of histidine biosynthesis to the control of free histidine concentrations in Arabidopsis thaliana. Plant Biotechnol. J. 7:499–511 [Google Scholar]
  160. Reinard T, Janke V, Willard J, Buck F, Jacobsen HJ, Vockley J. 160.  2000. Cloning of a gene for an acyl-CoA dehydrogenase from Pisum sativum L. and purification and characterization of its product as an isovaleryl-CoA dehydrogenase. J. Biol. Chem. 275:33738–43 [Google Scholar]
  161. Reisch B, Bingham ET. 161.  1981. Plants from ethionine-resistant alfalfa tissue cultures: variation in growth and morphological characteristics. Crop Sci. 21:783–88 [Google Scholar]
  162. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K. 162.  et al. 2009. In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol. 150:125–43 [Google Scholar]
  163. Reyes AR, Bonin CP, Houmard NM, Huang S, Malvar TM. 163.  2009. Genetic manipulation of lysine catabolism in maize kernels. Plant Mol. Biol. 69:81–89 [Google Scholar]
  164. Roje S. 164.  2006. S-Adenosyl-l-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–98 [Google Scholar]
  165. Rose AB, Beliakoff JA. 165.  2000. Intron-mediated enhancement of gene expression independent of unique intron sequences and splicing. Plant Physiol. 122:535–42 [Google Scholar]
  166. Roth JR, Ames BN. 166.  1966. Histidine regulatory mutants in Salmonella typhimurium. II. Histidine regulatory mutants having altered histidyl-tRNA synthetase. J. Mol. Biol. 22:325–33 [Google Scholar]
  167. Rowe HC, Hansen BG, Halkier BA, Kliebenstein DJ. 167.  2008. Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome. Plant Cell 20:1199–216 [Google Scholar]
  168. Sawada Y, Kuwahara A, Nagano M, Narisawa T, Sakata A. 168.  et al. 2009. Omics-based approaches to methionine side chain elongation in Arabidopsis: characterization of the genes encoding methylthioalkylmalate isomerase and methylthioalkylmalate dehydrogenase. Plant Cell Physiol. 50:1181–90 [Google Scholar]
  169. Schuster J, Binder S. 169.  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. 57:241–54 [Google Scholar]
  170. Schuster J, Knill T, Reichelt M, Gershenzon J, Binder S. 170.  2006. BRANCHED-CHAIN AMINOTRANSFERASE4 is of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18:2664–79 [Google Scholar]
  171. Semel Y, Schauer N, Roessner U, Zamir D, Fernie AR. 171.  2007. Metabolite analysis for the comparison of irrigated and non-irrigated field grown tomato of varying genotype. Metabolomics 3:289–95 [Google Scholar]
  172. Shaul O, Galili G. 172.  1992. Increased lysine synthesis in tobacco plants that express high levels of bacterial dihydrodipicolinate synthase in their chloroplasts. Plant J. 2:203–9 [Google Scholar]
  173. Shaul O, Galili G. 173.  1992. Threonine overproduction in transgenic tobacco plants expressing a mutant desensitized aspartate kinase of Escherichia coli. Plant Physiol. 100:1157–63 [Google Scholar]
  174. Shaul O, Galili G. 174.  1993. Concerted regulation of lysine and threonine synthesis in tobacco plants expressing bacterial feedback-insensitive aspartate kinase and dihydrodipicolinate synthase. Plant Mol. Biol. 23:759–68 [Google Scholar]
  175. Shen B, Li CJ, Tarczynski MC. 175.  2002. High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J. 29:371–80 [Google Scholar]
  176. Singh BK. 176.  1999. Biosynthesis of valine, leucine, and isoleucine. Plant Amino Acids: Biochemistry and Biotechnology BK Singh 227–47 New York: Dekker [Google Scholar]
  177. Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA. 177.  et al. 2008. Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiol. 148:1830–46 [Google Scholar]
  178. Sodek L, Wilson CM. 178.  1970. Incorporation of leucine-14C and lysine-14C into protein in developing endosperm of normal and opaque-2 corn. Arch. Biochem. Biophys. 140:29–38 [Google Scholar]
  179. Song S, Hou W, Godo I, Wu C, Yu Y. 179.  et al. 2013. Soybean seeds expressing feedback-insensitive cystathionine-synthase exhibit a higher content of methionine. J. Exp. Bot. 64:1917–26 [Google Scholar]
  180. Stepansky A, Less H, Angelovici R, Aharon R, Zhu X, Galili G. 180.  2006. Lysine catabolism, an effective versatile regulator of lysine level in plants. Amino Acids 30:121–25 [Google Scholar]
  181. Sweetlove LJ, Fernie AR. 181.  2013. The spatial organization of metabolism within the plant cell. Annu. Rev. Plant Biol. 64:723–46 [Google Scholar]
  182. Tan S, Evans R, Singh B. 182.  2006. Herbicidal inhibitors of amino acid biosynthesis and herbicide-tolerant crops. Amino Acids 30:195–204 [Google Scholar]
  183. Taylor NL, Heazlewood JL, Day DA, Millar AH. 183.  2004. Lipoic acid-dependent oxidative catabolism of α-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol. 134:838–48 [Google Scholar]
  184. Textor S, de Kraker J-W, Hause B, Gershenzon J, Tokuhisa JG. 184.  2007. MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol. 144:60–71 [Google Scholar]
  185. Thomazeau K, Curien G, Dumas R, Biou V. 185.  2001. Crystal structure of threonine synthase from Arabidopsis thaliana. Protein Sci. 10:638–48 [Google Scholar]
  186. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ. 186.  2006. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. PNAS 103:8287–92 [Google Scholar]
  187. Timm S, Wittmiss M, Gamlien S, Ewald R, Florian A. 187.  et al. 2015. Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. Plant Cell 27:1968–84 [Google Scholar]
  188. Tohge T, Watanabe M, Hoefgen R, Fernie AR. 188.  2013. The evolution of phenylpropanoid metabolism in the green lineage. Crit. Rev. Biochem. Mol. Biol. 48:123–52 [Google Scholar]
  189. Tohge T, Watanabe M, Hoefgen R, Fernie AR. 189.  2013. Shikimate and phenylalanine biosynthesis in the green lineage. Front. Plant Sci. 4:62 [Google Scholar]
  190. Tzin V, Galili G. 190.  2010. The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. Arabidopsis Book 8:e0132 [Google Scholar]
  191. Tzin V, Malitsky S, Aharoni A, Galili G. 191.  2009. Expression of a bacterial bi-functional chorismate mutase/prephenate dehydratase modulates primary and secondary metabolism associated with aromatic amino acids in Arabidopsis. Plant J. 60:156–67 [Google Scholar]
  192. Tzin V, Malitsky S, Ben Zvi MM, Bedair M, Sumner L. 192.  et al. 2012. Expression of a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in Arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. New Phytol. 194:430–39 [Google Scholar]
  193. Tzin V, Rogachev I, Meir S, Ben Zvi MM, Masci T. 193.  et al. 2013. Tomato fruits expressing a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway possess enhanced levels of multiple specialized metabolites and upgraded aroma. J. Exp. Bot. 64:4441–52 [Google Scholar]
  194. Vauterin M, Frankard V, Jacobs M. 194.  1999. The Arabidopsis thaliana dhdps gene encoding dihydrodipicolinate synthase, key enzyme of lysine biosynthesis, is expressed in a cell-specific manner. Plant Mol. Biol. 39:695–708 [Google Scholar]
  195. Wang B, Chu J, Yu T, Xu Q, Sun X. 195.  et al. 2015. Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. PNAS 112:4821–26 [Google Scholar]
  196. Ward E, Ohta D. 196.  1999. Histidine biosynthesis. Plant Amino Acids: Biochemistry and Biotechnology BK Singh 293–303 New York: Dekker [Google Scholar]
  197. Watanabe S, Hayashi K, Yagi K, Asai T, MacTavish H. 197.  et al. 2002. Biogenesis of 2-phenylethanol in rose flowers: incorporation of [2H8]l-phenylalanine into 2-phenylethanol and its β-d-glucopyranoside during the flower opening of Rosa “Hoh-Jun” and Rosa damascena Mill. Biosci. Biotechnol. Biochem. 66:943–47 [Google Scholar]
  198. 198. WHO (World Health Organ.) 2007. Protein and amino acid requirements in human nutrition Tech. Rep. Ser. 935, WHO, Geneva, Switz. [Google Scholar]
  199. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 199.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  200. Witt S, Galicia L, Lisec J, Cairns J, Tiessen A. 200.  et al. 2012. Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Mol. Plant 5:401–17 [Google Scholar]
  201. Yamada T, Matsuda F, Kasai K, Fukuoka S, Kitamura K. 201.  et al. 2008. Mutation of a rice gene encoding a phenylalanine biosynthetic enzyme results in accumulation of phenylalanine and tryptophan. Plant Cell 20:1316–29 [Google Scholar]
  202. Yamashita Y, Kadokura Y, Sotta N, Fujiwara T, Takigawa I. 202.  et al. 2014. Ribosomes in a stacked array. J. Biol. Chem. 289:12693–704 [Google Scholar]
  203. Yoo H, Widhalm JR, Qian Y, Maeda H, Cooper BR. 203.  et al. 2013. An alternative pathway contributes to phenylalanine biosynthesis in plants via a cytosolic tyrosine:phenylpyruvate aminotransferase. Nat. Commun. 42833 [Google Scholar]
  204. Zeh M, Casazza AP, Kreft O, Roessner U, Bieberich K. 204.  et al. 2001. Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol. 127:792–802 [Google Scholar]
  205. Zeier J. 205.  2013. New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ. 36:2085–103 [Google Scholar]
  206. Zhang C, Pang Q, Jiang L, Wang S, Yan X. 206.  et al. 2015. Dihydroxyacid dehydratase is important for gametophyte development and disruption causes increased susceptibility to salinity stress in Arabidopsis. J. Exp. Bot. 66:879–88 [Google Scholar]
  207. Zhu X, Galili G. 207.  2003. Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15:845–53 [Google Scholar]
  208. Zhu X, Galili G. 208.  2004. Lysine metabolism is concurrently regulated by synthesis and catabolism in both reproductive and vegetative tissues. Plant Physiol. 135:129–36 [Google Scholar]
  209. Zhu-Shimoni JX, Galili G. 209.  1998. Expression of an Arabidopsis aspartate kinase homoserine dehydrogenase gene is metabolically regulated by photosynthesis-related signals but not by nitrogenous compounds. Plant Physiol. 116:1023–28 [Google Scholar]
  210. Zhu-Shimoni JX, Lev-Yadun S, Matthews B, Galili G. 210.  1997. Expression of an aspartate kinase homoserine dehydrogenase gene is subject to specific spatial and temporal regulation in vegetative tissues, flowers, and developing seeds. Plant Physiol. 113:695–706 [Google Scholar]
  211. Zinnanti WJ, Lazovic J, Housman C, LaNoue K, O'Callaghan JP. 211.  et al. 2007. Mechanism of age-dependent susceptibility and novel treatment strategy in glutaric acidemia type I. J. Clin. Investig. 117:3258–70 [Google Scholar]
  212. Zrenner R, Stitt M, Sonnewald U, Boldt R. 212.  2006. Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57:805–36 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043015-112213
Loading
The Regulation of Essential Amino Acid Synthesis and Accumulation in Plants
Annual Review of Plant Biology 67, 153 (2016); https://doi.org/10.1146/annurev-arplant-043015-112213
/content/journals/10.1146/annurev-arplant-043015-112213
/content/journals/10.1146/annurev-arplant-043015-112213
Loading

Data & Media loading...

Supplementary Data

  • Download Supplemental Table 1 as a PDF.

    Download Supplemental Figures 1–3 as a single PDF, or see below:

    Supplemental Figure 1. The biosynthesis pathway of His biosynthesis in plants. Black arrows indicated reactions, the grey arrow with a “minus” represents a feedback inhibitory loop. Enzymes are represented by numbers: 1, ribose-phosphate diphosphokinase; 2, ATP-phosphoribosyltransferase; 3, phosphoribosyl-ATP pyrophosphohydrolase; 4, phosphoribosyl-AMP cyclohydrolase; 5, N´-[(5´-phosphoribosyl)formimino]-5-aminoimidazole-4-carboxamide ribonucleotide isomerase; 6, Imidazole glycerol-phosphate synthase; 7, imidazole glycerol-phosphate dehydratase; 8, histidinol-phosphate aminotransferase; 9, histidinol-phosphate phosphatase; 10, histidinol dehydrogenase.

    Supplemental Figure 2. Lys degradation in plants. The route on the left represents the better characterized route in plants; however, the pathway on the right is similar to that identified in Rhodospirillum and also clearly contributes to plant Lys degradation. Broken arrows represent non-specified enzymatic reactions. 2-OG, 2-oxoglutarate. Enzymes are demarcated with numbers: 1, Lys glutarate reductase; 2, saccharophine dehydrogenase; 3 aminoadipate semialdehyde dehydrogenase; 4 aminoadipate aminotransferase; 5, a general  amino acid transferase; 6 D-2 hydroxyglutarate dehydrogenase.

    Supplemental Figure 3. Branched chain amino acid  degradation. Enzymes are demarcated with numbers: 1, branched chain amino transferase;  2, 3-methyl-2-oxobutanoate dehydrogenase;  3, acyltransferase transferring groups other than amino-acyl groups;  4; acyl-CoA dehydrogenase; 5, methylcrotonyl-CoA carboxylase; 6, enoyl-CoA hydratase; 7, 3-methylglutaconyl-CoA hydratase; 8, 3-hydroxyisobutyryl-CoA hydrolase; 9, 3-hydroxyacyl-CoA dehydrogenase; 10, hydroxymethylglutaryl-CoA synthase; 11, 3-ketoacyl-CoA thiolase; 12, aldehyde oxidase; 13, aldehyde dehydrogenase; 14, hydroxymethylglutaryl-CoA lyase.

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error