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Biosynthetic pathway of shikimate and aromatic amino acid and its metabolic engineering in plants

식물에서 shikimate 및 방향족 아미노산 생합성 경로와 이의 대사공학적 응용

  • Lim, Sun-Hyung (National Academy of Agricultural Science, Rural Development Administration) ;
  • Park, Sang Kyu (National Academy of Agricultural Science, Rural Development Administration) ;
  • Ha, Sun-Hwa (Graduate School of Biotechnology, Kyung Hee University) ;
  • Choi, Min Ji (National Academy of Agricultural Science, Rural Development Administration) ;
  • Kim, Da-Hye (National Academy of Agricultural Science, Rural Development Administration) ;
  • Lee, Jong-Yeol (National Academy of Agricultural Science, Rural Development Administration) ;
  • Kim, Young-Mi (National Academy of Agricultural Science, Rural Development Administration)
  • 임선형 (국립농업과학원, 농촌진흥청) ;
  • 박상규 (국립농업과학원, 농촌진흥청) ;
  • 하선화 (생명공학원, 경희대학교) ;
  • 최민지 (국립농업과학원, 농촌진흥청) ;
  • 김다혜 (국립농업과학원, 농촌진흥청) ;
  • 이종렬 (국립농업과학원, 농촌진흥청) ;
  • 김영미 (국립농업과학원, 농촌진흥청)
  • Received : 2015.04.14
  • Accepted : 2015.05.29
  • Published : 2015.09.30

Abstract

The aromatic amino acids, which are composed of $\small{L}$-phenylalanine, $\small{L}$-tyrosine and $\small{L}$-tryptophan, are general components of protein synthesis as well as precursors for a wide range of secondary metabolites. These aromatic amino acids-derived compounds play important roles as ingredients of diverse phenolics including pigments and cell walls, and hormones like auxin and salicylic acid in plants. Moreover, they also serve as the natural products of alkaloids and glucosinolates, which have a high potential to promote human health and nutrition. The biosynthetic pathways of aromatic amino acids share a chorismate, the common intermediate, which is originated from shikimate pathway. Then, tryptophan is synthesized via anthranilate and the other phenylalanine and tyrosine are synthesized via prephenate, as intermediates. This review reports recent studies about all the enzymatic steps involved in aromatic amino acid biosynthetic pathways and their gene regulation on transcriptional/post-transcriptional levels. Furthermore, results of metabolic engineering are introduced as efforts to improve the production of the aromatic amino acids-derived secondary metabolites in plants.

식물의 페닐알라닌, 티로신, 그리고 트립토판과 같은 방향족 아미노산은 단백질 합성의 구성 성분 뿐만 아니라 다양한 이차 대사물질들의 전구물질들이다. 이러한 방향족 아미노산 유래의 화합물들은 식물의 색소와 세포벽 구성성분을 포함하는 다양한 페놀릭 화합물들의 구성성분이자, 옥신과 살리실산과 같은 식물 호르몬으로써 중요한 역할을 수행한다. 또한 이들은 인간의 영양과 건강을 증진하는 높은 잠재력을 지니는 알칼로이드 및 글루코시놀레이트와 같은 천연산물로써 역할을 한다. 방향족 아미노산의 생합성경로는 shikimate 경로로부터 유래되는 공통의 중간기질인 chorismate를 공유한다. 트립토판은 중간기질로 anthranilate를 통해 합성되고, 페닐알라닌 및 티로신은 중간기질인 prephenate를 통해 합성된다. 본 논문에서는 방향족 아미노산 생합성경로에 관련한 모든 단계의 효소와 전사/전사후 수준에서의 그들의 유전자 조절에 대한 최근 연구들에 대해 종합적으로 되짚어 보면서, 추가적으로 식물의 방향족 아미노산 유래의 천연물질 생산을 증진시키기 위해 그 동안 시도되어온 대사 공학적 노력들에 대해서 소개하고자 한다.

Keywords

References

  1. Anton IA, Coggins JR (1988) Sequencing and overexpression of the Escherichia coli aroE gene encoding shikimate dehydrogenase. Biochem J 249:319-326 https://doi.org/10.1042/bj2490319
  2. Arabidopsis Genome Initiat (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815 https://doi.org/10.1038/35048692
  3. Barends TRM, Dunn MF, Schlichting I (2008) Tryptophan synthase, an allosteric molecular factory. Curr Opin Chem Biol 12:593-600 https://doi.org/10.1016/j.cbpa.2008.07.011
  4. Bartee L, Bender J (2001) Two Arabidopsis methylation-deficiency mutations confer only partial effects on a methylated endogenous gene family. Nucleic Acids Res 29:2127-2134 https://doi.org/10.1093/nar/29.10.2127
  5. Basset G, Quinlivan E, Ravanel S, Rebeille F, Nichols B, Shinozaki K, Seki M, Adams-Phillips L, Giovannoni J, Gregory J, Hanson A (2004) Folate synthesis in plants: the p-aminobenzoate branch is initiated by a bifunctional PabA-PabB protein that is targeted to plastids. Proc Natl Acad Sci USA 101:1496-1501 https://doi.org/10.1073/pnas.0308331100
  6. Benesova M, Bode R (1992) Chorismate mutase isoforms from seeds and seedlings of Papaver somniferum. Phytochemistry 31:2983-2987 https://doi.org/10.1016/0031-9422(92)83431-W
  7. Benfey PN, Chua NH (1989) Regulated genes in transgenic plants. Science 244:174-181 https://doi.org/10.1126/science.244.4901.174
  8. Bentley R (1990) The shikimate pathway a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307-384 https://doi.org/10.3109/10409239009090615
  9. Bischoff M, Rosler J, Raesecke HR, Gorlach J, Amrhein N, Schmid J (1996) Cloning of a cDNA encoding a 3-dehydroquinate synthase from a higher plant, and analysis of the organ-specific and elicitor-induced expression of the corresponding gene. Plant Mol Biol 31:69-76 https://doi.org/10.1007/BF00020607
  10. Bischoff M, Schaller A, Bieri F, Kessler F, Amrhein N, Schmid J (2001) Molecular characterization of tomato 3-dehydroquinate dehydratase-shikimate: NADP oxidoreductase. Plant Physiol 125:1891-1900 https://doi.org/10.1104/pp.125.4.1891
  11. Bohlmann J, DeLuca V, Eilert U, Martin W (1995) Purification and cDNA cloning of anthranilate synthase from Ruta graveolens: modes of expression and properties of native and recombinant enzymes. Plant J 7:491-501 https://doi.org/10.1046/j.1365-313X.1995.7030491.x
  12. Bonner CA, Jensen RA (1985) Novel features of prephenate aminotransferase from cell cultures of Nicotiana silvestris. Arch Biochem Biophys 238:237-246 https://doi.org/10.1016/0003-9861(85)90161-4
  13. Chibani K, Ali-Rachedi S, Job C, Job D, Jullien M, Grappin P (2006) Proteomic analysis of seed dormancy in Arabidopsis. Plant Physiol 142:1493-1510 https://doi.org/10.1104/pp.106.087452
  14. Cho HJ, Brotherton JE, Song HS, Widholm JM (2000) Increasing tryptophan synthesis in a forage legume Astragalus sinicus by expressing the tobacco feedback-insensitive anthranilate synthase (ASA2) gene. Plant Physiol 123:1069-1076 https://doi.org/10.1104/pp.123.3.1069
  15. Cho M, Corea O, Yang H, Bedgar D, Laskar D, Anterola A, Moog-Anterola F, Hood R, Kohalmi S, Bernards M, Kang C, Davin L, Lewis N (2007) Phenylalanine biosynthesis in Arabidopsis thaliana identification and characterization of Arogenate dehydratases. J Biol Chem 282:30827-30835 https://doi.org/10.1074/jbc.M702662200
  16. Chook YM, Ke H, Lipscomb WN (1993) Crystal structures of the monofunctional chorismate mutase from Bacillus subtilis and its complex with a transition state analog. Proc Natl Acad Sci USA 90:8600-8603 https://doi.org/10.1073/pnas.90.18.8600
  17. Colquhoun TA, Schimmel BCJ, Kim JY, Reinhardt D, Cline K, Clark DG (2010a) A petunia chorismate mutase specialized for the production of floral volatiles. Plant J 61:145-155 https://doi.org/10.1111/j.1365-313X.2009.04042.x
  18. Colquhoun TA, Verdonk JC, Schimmel BC, Tieman DM, Underwood BA, Clark DG (2010b) Petunia floral volatile benzenoid/ phenylpropanoid genes are regulated in a similar manner. Phytochem 71:158-167 https://doi.org/10.1016/j.phytochem.2009.09.036
  19. Connelly JA, Conn EE (1986) Tyrosine biosynthesis in Sorghum bicolor: isolation and regulatory properties of arogenate dehydrogenase. Z Naturforsch C 41:69-78
  20. d'Amato T, Ganson R, Gaines C, Jensen R (1984) Subcellular localization of chorismate-mutase isoenzymes in protoplasts from mesophyll and suspension-cultured cells of Nicotiana silvestris. Planta 162:104-108 https://doi.org/10.1007/BF00410205
  21. Devoto A, Ellis C, Magusin A, Chang H, Chilcott C, Zhu T, Turner J (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonateinduced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497-513 https://doi.org/10.1007/s11103-005-7306-5
  22. Ding L, Hofius D, Hajirezaei M-R, Fernie AR, Bornke F, Sonnewald U (2007) Functional analysis of the essential bifunctional tobacco enzyme 3-dehydroquinate dehydratase/shikimate dehydrogenase in transgenic tobacco plants. J Exp Bot 58:2053-2067 https://doi.org/10.1093/jxb/erm059
  23. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R (2011) Metabolic priming by a secreted fungal effector. Nature 478:395-398 https://doi.org/10.1038/nature10454
  24. Dombrecht B, Xuea GP, Spragueb SJ, Kirkegaardb JA, Rossc JJ, Reidc JB, Fittd GP, Sewelama N, Schenke PM, Mannersa JM, Kazana K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225-2245 https://doi.org/10.1105/tpc.106.048017
  25. Doong RL, Ganson RJ, Jensen RA (1993) Plastid-localized 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DS-Mn): the early-pathway target of sequential feedback inhibition in higher plants. Plant Cell Environ 16:393-402 https://doi.org/10.1111/j.1365-3040.1993.tb00885.x
  26. Dornfeld C, Weisberg AJ, Ritesh KC, Dudareva N, Jelesko JG, Maeda HA (2014) Phylobiochemical characterization of class-Ib aspartate/prephenate aminotransferases reveals evolution of the plant arogenate phenylalanine pathway. Plant Cell 26:3101-3114 https://doi.org/10.1105/tpc.114.127407
  27. Duncan K, Edwards RM, Coggins JR (1987) The pentafunctional arom enzyme of Saccharomyces cerevisiae is a mosaic of monofunctional domains. Biochem J 246:375-386 https://doi.org/10.1042/bj2460375
  28. Dyer WE, Weaver LM, Zhao JM, Kuhn DN, Weller SC, Herrmann KM (1990) A cDNA encoding 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase from Solanum tuberosum L. J Biol Chem 265:1608-1614
  29. Eberhard J, Ehrler TT, Epple P, Felix G, Raesecke HR, Amrhein N, Amrhein J (1996) Cytosolic and plastidic chorismate mutase isozymes from Arabidopsis thaliana: molecular characterization and enzymatic properties. Plant J 10:815-821 https://doi.org/10.1046/j.1365-313X.1996.10050815.x
  30. Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis IF, Zhuang J, Kaneda M, Mansfield SD, Samuels L, Ritland K, Ellis BE, Bohlmann J, Douglas CJ (2005) Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42:618-640 https://doi.org/10.1111/j.1365-313X.2005.02403.x
  31. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978-984 https://doi.org/10.1110/ps.8.5.978
  32. Entus R, Poling M, Herrmann KM (2002) Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase. Plant Physiol 129:1866-1871 https://doi.org/10.1104/pp.002626
  33. Falk J, Andersen G, Kernebeck B, Krupinska K (2003) Constitutive overexpression of barley 4-hydroxyphenylpyruvate dioxygenase in tobacco results in elevation of the vitamin E content in seeds but not in leaves. FEBS Lett 540:35-40 https://doi.org/10.1016/S0014-5793(03)00166-2
  34. Fiedler E, Schultz G (1985) Localization, purification, and characterization of shikimate oxidoreductase dehydroquinate hydrolyase from stroma of spinach chloroplasts. Plant Physiol 79:212-218 https://doi.org/10.1104/pp.79.1.212
  35. Forlani G, Parisi B, Nielsen E (1994) 5-Enol-pyruvyl-shikimate- 3-phosphate synthase from Zea mays cultured cells (purification and properties). Plant Physiol 105:1107-1114 https://doi.org/10.1104/pp.105.4.1107
  36. Fucile G, Garcia C, Carlsson J, Sunnerhagen M, Christendat D (2011) Structural and biochemical investigation of two Arabidopsis shikimate kinases: The heat-inducible isoform is thermostable. Protein Sci 20:1125-1136 https://doi.org/10.1002/pro.640
  37. Funke T, Han H, Healy-Fried ML, Fischer M, Schonbrunn E (2006) Molecular basis for the herbicide resistance of Roundup Ready crops. Proc Natl Acad Sci USA 103:13010-13015 https://doi.org/10.1073/pnas.0603638103
  38. Galili G, Hoefgen R (2002) Metabolic engineering of amino acids and storage proteins in plants. Metab Eng 4:3-11 https://doi.org/10.1006/mben.2001.0203
  39. Garg B, Vaid N, Tuteja N (2014) In-silico analysis and expression profiling implicate diverse role of EPSPS family genes in regulating developmental and metabolic processes. BMC Res Notes 7:58 https://doi.org/10.1186/1756-0500-7-58
  40. Gasser CS, Winter JA, Hironaka CM, Shah DM (1988) Structure, expression, and evolution of the 5-enolpyruvylshikimate- 3-phosphate synthase genes of petunia and tomato. J Biol Chem 263:4280-4287
  41. Gilchrist DG, Woodin TS, Johnson ML, Kosuge T (1972) Regulation of aromatic amino acid biosynthesis in higher plants: I. Evidence for a regulatory form of chorismate mutase in etiolated mung bean seedlings. Plant Physiol 49:52-57 https://doi.org/10.1104/pp.49.1.52
  42. Gorlach J, Raesecke H, Rentsch D, Regenass M, Roy P, Zala M, Kell C, Boller T, Amrhein N, Schmid J (1995) Temporally distinct accumulation of transcripts encoding enzymes of the prechorismate pathway in elicitor-treated, cultured tomato cells. Proc Natl Acad Sci USA 92:3166-3170 https://doi.org/10.1073/pnas.92.8.3166
  43. Gorlach J, Schmid J, Amrhein N (1993) Differential expression of tomato (Lycopersicon esculentum L.) genes encoding shikimate pathway isoenzymes. II. Chorismate synthase. Plant Mol Biol 23:707-716 https://doi.org/10.1007/BF00021526
  44. Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K, Shinozaki K, Seki M, Herrmann RG, Meurer J (2006) A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J Biol Chem 281:17189-17196 https://doi.org/10.1074/jbc.M601754200
  45. Hamberger B, Ehlting J, Barbazuk B, Douglas CJ (2006) Comparative genomics of the shikimate pathway in Arabidopsis, Populus trichocarpa and Oryza sativa: shikimate pathway gene family structure and identification of candidates for missing links in phenylalanine biosynthesis. Recent Adv Phytochem 40:85-113 https://doi.org/10.1016/S0079-9920(06)80038-9
  46. He Y, Li J (2001) Differential expression of triplicate phosphoribosylanthranilate isomerase isogenes in the tryptophan biosynthetic pathway of Arabidopsis thaliana (L.) Heynh. Planta 212:641-647 https://doi.org/10.1007/s004250000452
  47. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473-503 https://doi.org/10.1146/annurev.arplant.50.1.473
  48. Holding DR, Meeley RB, Hazebroek J, Selinger D, Gruis F, Jung RF, Larkins BA (2010) Identification and characterization of the maize arogenate dehydrogenase gene family. J Exp Bot 61:3663-3673 https://doi.org/10.1093/jxb/erq179
  49. Huang L, Montoya AL, Nester EW (1975) Purification and characterization of shikimate kinase enzyme activity in Bacillus subtilis. J Biol Chem 250:7675-7681
  50. Hughes EH, Hong SB, Gibson SI, Shank JV, San KY (2004) Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab Eng 6:268-276 https://doi.org/10.1016/j.ymben.2004.03.002
  51. Huisman OC, Kosuge T (1974) Regulation of aromatic amino acid biosynthesis in higher plants. II. 3-deoxy-arabino-heptulosonic acid 7-phosphate synthetase from cauliflower. J Biol Chem 249:6842-6848
  52. Huynb QK, Kisbore GM, Bild GS (1998) 5-enolpyruvyl shikimate- 3-phosphate synthase from Escherichia coli: identification of Lys-22 as a potential active site residue. J Biol Chem 263:735-739
  53. Ishihara A, Asada Y, Takahashi Y, Yabe N, Komeda Y, Nishioka T, Miyagawaa H, Wakasab K (2006) Metabolic changes in Arabidopsis thaliana expressing the feedback-resistant anthranilate synthase alpha subunit gene OASA1D. Phytochemistry 67: 2349-2362 https://doi.org/10.1016/j.phytochem.2006.08.008
  54. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138:790-802 https://doi.org/10.1104/pp.105.062778
  55. Jones PR, Manabe T, Awazuhara M, Saito K (2003) A new member of plant CS-lyases: a cystine lyase from Arabidopsis thaliana. J Biol Chem 278:10291-10296 https://doi.org/10.1074/jbc.M212207200
  56. Jung E, Zamir LO, Jensen RA (1986) Chloroplasts of higher plants synthesize L-phenylalanine via Larogenate. Proc Natl Acad Sci USA 83:7231-7235 https://doi.org/10.1073/pnas.83.19.7231
  57. Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G, Weiss D, Orlova I, Lavie O, Rhodes D, Wood K, Porterfi eld DM, Cooper AJ, Schloss JV, Pichersky E, Vainstein A, Dudareva N (2006) Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J Biol Chem 281:23357-23366 https://doi.org/10.1074/jbc.M602708200
  58. Kasai K, Kanno T, Akita M, Ikejiri-Kanno Y, Wakasa K, Tozawa Y (2005) Identification of three shikimate kinase genes in rice: characterization of their differential expression during panicle development and of the enzymatic activities of the encoded proteins. Planta 222:438-447 https://doi.org/10.1007/s00425-005-1559-8
  59. Kaur H, Heinzel N, Schottner M, Baldwin IT, Galis I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoidpolyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731-1747 https://doi.org/10.1104/pp.109.151738
  60. Keith B, Dong X, Ausubel F, Fink G (1991) Differential induction of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase genes in Arabidopsis thaliana by wounding and pathogenic attack. Proc Natl Acad Sci USA 88:8821-8825 https://doi.org/10.1073/pnas.88.19.8821
  61. Kim H, van Oostende C, Basset G, Browse J (2008) The AAE14 gene encodes the Arabidopsis o-succinylbenzoyl-CoA ligase that is essential for phylloquinone synthesis and photosystem-I function. Plant J 54:272-283 https://doi.org/10.1111/j.1365-313X.2008.03416.x
  62. Klee HJ, Muskopf YM, Gasser CS (1987) Cloning of an Arabidopsis thaliana gene encoding 5-enolpyruvylshikimate-3-phosphate synthase: sequence analysis and manipulation to obtain glyphosate tolerant plants. Mol Gen Genet 210:437-442 https://doi.org/10.1007/BF00327194
  63. Kleeb AC, Kast P, Hilvert D (2006) A monofunctional and thermostable prephenate dehydratase from the archaeon Methanocaldococcus jannaschii. Biochemistry 45:14101-14110 https://doi.org/10.1021/bi061274n
  64. Knaggs AR (2001) The biosynthesis of shikimate metabolites. Nat Prod Rep 18:334-355 https://doi.org/10.1039/b001717p
  65. Kriechbaumer V, Weigang L, Fiesselmann A, Letzel T, Frey M, Gierl A, Glawischnig E (2008) Characterisation of the tryptophan synthase alpha subunit in maize. BMC Plant Biol 8:44 https://doi.org/10.1186/1471-2229-8-44
  66. Kuroki GW, Conn EE (1989) Differential activities of chorismate mutase isozymes in tubers and leaves of Solanum tuberosum L. Plant Physiol 89:472-476 https://doi.org/10.1104/pp.89.2.472
  67. Lee AY, Karplus PA, Ganem B, Clardy J (1995) Atomic structure of the buried catalytic pocket of Escherichia coli chorismate mutase. J Am Chem Soc 117:3627-3628 https://doi.org/10.1021/ja00117a038
  68. Legrand P, Dumas R, Seux M, Rippert P, Ravelli R, Ferrer JL, Matringe M (2006) Biochemical characterization and crystal structure of Synechocystis arogenate dehydrogenase provide insights into catalytic reaction. Structure 14:767-776 https://doi.org/10.1016/j.str.2006.01.006
  69. Leonard E, Runguphan W, O'Connor S, Prather KJ (2009) Opportunities in metabolic engineering to facilitate scalable alkaloid production. Nat Chem Biol 5:292-300 https://doi.org/10.1038/nchembio.160
  70. Lepiniec L, Debeaujon L, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405-430 https://doi.org/10.1146/annurev.arplant.57.032905.105252
  71. Li J, Last RL (1996) The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol 110:51-59 https://doi.org/10.1104/pp.110.1.51
  72. Li J, Zhao J, Rose AB, Schmidt R, Last RL (1995b) Arabidopsis phosphoribosylanthranilate isomerase: molecular genetic analysis of triplicate tryptophan pathway genes. Plant Cell 7:447-461 https://doi.org/10.1105/tpc.7.4.447
  73. Li J, Chen S, Zhu L, Last RL (1995a) Isolation of cDNAs encoding the tryptophan pathway enzyme indole-3-glycerol phosphate synthase from Arabidopsis thaliana. Plant Physiol 1088(1): 877-878
  74. Lopukhina A, Dettenberg M, Weiler EW, Hollander-Czytko H (2001) Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiol 126:1678-1687 https://doi.org/10.1104/pp.126.4.1678
  75. Macheroux P, Schmid J, Amrhein N, Schaller A (1999) A unique reaction in a common pathway: mechanism and function of chorismate synthase in the shikimate pathway. Planta 207:325-334 https://doi.org/10.1007/s004250050489
  76. Maclean J, Ali S (2003) The structure of chorismate synthase reveals a novel flavin binding site fundamental to a unique chemical reaction. Structure 11:1499-1511 https://doi.org/10.1016/j.str.2003.11.005
  77. Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol 63:73-105 https://doi.org/10.1146/annurev-arplant-042811-105439
  78. Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooperd BR, Rhodesa D, Picherskyc E, Dudarevaa N (2010) RNAi suppression of Arogenate Dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals. Plant Cell 22:832-849 https://doi.org/10.1105/tpc.109.073247
  79. Maeda H, Yoo H, Dudareva N (2011) Prephenate aminotransferase directs plant phenylalanine biosynthesis via arogenate. Nat Chem Biol 7:19-21 https://doi.org/10.1038/nchembio.485
  80. Malitsky S, Blum E, Less H, Venger I, Elbaz M, Morin S, Eshed Y, Aharoni A (2008) The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol 148:2021-2049 https://doi.org/10.1104/pp.108.124784
  81. Matsuda F, Yamada T, Miyazawa H, Miyagawa H, Wakasa K (2005) Characterization of tryptophan overproducing potato transgenic for a mutant rice anthranilate synthase alpha-subunit gene (OASA1D). Planta 222:535-545 https://doi.org/10.1007/s00425-005-1565-x
  82. Melquist S, Bender J (2003) Transcription from an upstream promoter controls methylation signaling from an inverted repeat of endogenous genes in Arabidopsis. Genes Dev 17:2036-2047 https://doi.org/10.1101/gad.1081603
  83. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozakib K, Ohme-Takagia M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270-280 https://doi.org/10.1105/tpc.106.047043
  84. Mobley E, Kunkel B, Keith B (1999) Identification, characterization and comparative analysis of a novel chorismate mutase gene in Arabidopsis thaliana. Gene 240:115-123 https://doi.org/10.1016/S0378-1119(99)00423-0
  85. Morino K, Matsuda F, Miyazawa H, Sukegawa A, Miyagawa H, Wakasa K (2005) Metabolic profiling of tryptophanoverproducing rice calli that express a feedback-insensitive alpha subunit of anthranilate synthase. Plant Cell Physiol 46:514-521 https://doi.org/10.1093/pcp/pci051
  86. Morollo AA, Eck MJ (2001) Structure of the cooperative allosteric anthranilate synthase from Salmonella typhimurium. Nat Struct Biol 8:243-247 https://doi.org/10.1038/84988
  87. Mousdale DM, Coggins JR (1986) Detection and subcellular localization of a higher plant chorismate synthase. FEBS Lett 205:328-332 https://doi.org/10.1016/0014-5793(86)80922-X
  88. Niyogi KK, Fink GR (1992) Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell 4:721-733 https://doi.org/10.1105/tpc.4.6.721
  89. Nobe Y, Kawaguchi S, Ura H, Nakai T, Hirotsu K, Kato R, Kuramitsu S (1998) The novel substrate recognition mechanism utilized by aspartate aminotransferase of the extreme thermophile Thermus thermophilus HB8. J Biol Chem 273:29554-29564 https://doi.org/10.1074/jbc.273.45.29554
  90. Oliva M, Ovadia R, Perl A, Bar E, Lewinsohn E, Galili G, Shamir MO (2015) Enhanced formation of aromatic amino acids increases fragrance without affecting flower longevity or pigmentation in Petunia$\times$ hybrida. Plant J 13:125-136
  91. Ouyang J, Shao X, Li J (2000) Indole-3-glycerol phosphate, a branch point of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant J 24:327-333 https://doi.org/10.1046/j.1365-313x.2000.00883.x
  92. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603-614 https://doi.org/10.1242/dev.01595
  93. Pingsha H, Yan H, Roger PW (2009) Functional contribution of chorismate synthase, anthranilate synthase, and chorismate mutase to penetration resistance in barley-powdery mildew interactions. MPMI 22:311-320 https://doi.org/10.1094/MPMI-22-3-0311
  94. Pinto JE, Suzich JA, Herrmann KM (1986) 3-Deoxy-D-arabinoheptulosonate 7-phosphate synthase from potato tuber (Solanum tuberosum L.). Plant Physiol 82:1040-1044 https://doi.org/10.1104/pp.82.4.1040
  95. Prabhu PR, Hudson AO (2010) Identification and partial characterization of an L-tyrosine aminotransferase (TAT) from Arabidopsis thaliana. Biochem Res Int 2010:549-572
  96. Quevillon-Cheruel S, Leulliot N, Meyer P, Graille M, Bremang M, Blondeau K, Sorel I, Poupon A, Janin J, van Tilbeurgh H (2004) Crystal structure of the bifunctional chorismate synthase from Saccharomyces cerevisiae. J Biol Chem 279:619-625 https://doi.org/10.1074/jbc.M310380200
  97. Radwanski ER, Barczak AJ, Last RL (1996) Characterization of tryptophan synthase alpha subunit mutants of Arabidopsis thaliana. Mol Gen Genet 253:353-361
  98. Radwanski ER, Last RL (1995a) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:921-934 https://doi.org/10.1105/tpc.7.7.921
  99. Radwanski ER, Zhao J, Last RL (1995b) Arabidopsis thaliana tryptophan synthase alpha: gene cloning, expression, and subunit interaction. Mol Gen Genet 248:657-667 https://doi.org/10.1007/BF02191705
  100. Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910-923 https://doi.org/10.1104/pp.106.082057
  101. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63-70
  102. Reinink M, Borstlap AC (1982) 3-Deoxy-D-arabino-heptulosonate 7-phosphate synthase from pea leaves: inhibition by L-tyrosine. Plant Sci Lett 26:167-171 https://doi.org/10.1016/0304-4211(82)90088-8
  103. Rippert P, Matringe M (2002) Purification and kinetic analysis of the two recombinant arogenate dehydrogenase isoforms of Arabidopsis thaliana. Eur J Biochem 269:4753-4761 https://doi.org/10.1046/j.1432-1033.2002.03172.x
  104. Rippert P, Scimemi C, Dubald M, Matringe M (2004) Engineering plant shikimate pathway for production of tocotrienol and improving herbicide resistance. Plant Physiol 134:92-100 https://doi.org/10.1104/pp.103.032441
  105. Rippert P, Puyaubert J, Grisollet D, Derrier L, Matringe M (2009) Tyrosine and phenylalanine are synthesized within the plastids in Arabidopsis. Plant Physiol 149:1251-1260 https://doi.org/10.1104/pp.108.130070
  106. Romero RM, Roberts MF, Phillipson JD (1995a) Anthranilate synthase in microorganisms and plants. Phytochemistry 39: 263-276 https://doi.org/10.1016/0031-9422(95)00010-5
  107. Romero RM, Roberts MF, Phillipson JD (1995b) Chorismate mutase in microorganisms and plants. Phytochemistry 40: 1015-1025 https://doi.org/10.1016/0031-9422(95)00408-Y
  108. Rose A, Casselman A, Last RL (1992) A phosphoribosylanthranilate transferase gene is defective in blue fluorescent Arabidopsis thaliana tryptophan mutants. Plant Physiol 100:582-592 https://doi.org/10.1104/pp.100.2.582
  109. Rose AB, Last RL (1997a) Introns act post-transcriptionally to increase expression of the Arabidopsis thaliana tryptophan pathway gene PAT1. Plant J 11:455-464 https://doi.org/10.1046/j.1365-313X.1997.11030455.x
  110. Rose AB, Li J, Last RL (1997b) An allelic series of blue fluorescent trp1 mutants of Arabidopsis thaliana. Genetics 145:197-205
  111. Rubin JL, Jensen RA (1979) Enzymology of L-tyrosine biosynthesis in mung bean (Vigna radiata [L.] Wilczek). Plant Physiol 64:727-734 https://doi.org/10.1104/pp.64.5.727
  112. Rubin JL, Jensen RA (1985) Differentially regulated isozymes of 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase from seedlings of Vigna radiata [L.] Wilczek. Plant Physiol 79:711-718 https://doi.org/10.1104/pp.79.3.711
  113. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defense compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653-668 https://doi.org/10.1111/j.1365-313X.2005.02560.x
  114. Schaller A, Schmid J, Leibinger U, Amrhein N (1991a) Molecular cloning and analysis of a cDNA coding for chorismate synthase from the higher plant Corydalis sempervirens Pers. J Biol Chem 266:21434-21438
  115. Schaller A, van Afferden M, Windhofer V, Bulow S, Abel G, Schmid J, Amrhein N (1991b) Purification and characterization of chorismate synthase from Euglena gracilis: comparison with chorismate synthases of plant and microbial origin. Plant Physiol 97:1271-1279 https://doi.org/10.1104/pp.97.4.1271
  116. Schmid J, Schaller A, Leibinger U, Boll W, Amrhein N (1992) The in-vitro synthesized tomato shikimate kinase precursor is enzymatically active and is imported and processed to the mature enzyme by chloroplasts. Plant J 2:375-383
  117. Siehl DL, Conn EE (1988) Kinetic and regulatory properties of arogenate dehydratase in seedlings of Sorghum bicolor (L.) Moench. Arch Biochem Biophys 260:822-829 https://doi.org/10.1016/0003-9861(88)90513-9
  118. Singh SA, Christendat D (2006) Structure of Arabidopsis dehydroquinate dehydratase-shikimate dehydrogenase and implications for metabolic channeling in the shikimate pathway. Biochemistry 45:7787-7796 https://doi.org/10.1021/bi060366+
  119. Spitzer-Rimon B, Marhevka E, Barkai O, Marton I, Edelbaum O, Masci T, Prathapani NK, Shklarman E, Ovadis M, Vainstein A (2010) EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles' biosynthesis in petunia. Plant Cell 22:1961-1976 https://doi.org/10.1105/tpc.109.067280
  120. Stenmark SL, Pierson DL, Jensen RA, Glover GI (1974) Blue-green bacteria synthesise L-tyrosine by the pre-tyrosine pathway. Nature 247:290-292 https://doi.org/10.1038/247290a0
  121. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660-677 https://doi.org/10.1111/j.1365-313X.2007.03078.x
  122. Suzich JA, Dean JF, Herrmann KM (1985) 3-Deoxy-D-arabinoheptulosonate 7-phosphate synthase from carrot root (Daucus carota) is a hysteretic enzyme. Plant Physiol 79:765-770 https://doi.org/10.1104/pp.79.3.765
  123. Tohge T, Watanabe M, Hoefgen R, Fernie AR (2013) Shikimate and phenylalanine biosynthesis in the green lineage. Front Plant Sci 4:62
  124. Tozawa Y, Hasegawa H, Terakawa T, Wakasa K (2001) Characterization of rice anthranilate synthase alpha-subunit genes OASA1 and OASA2: tryptophan accumulation in transgenic rice expressing a feedback-insensitive mutant of OASA1. Plant Physiol 126:1493-1506 https://doi.org/10.1104/pp.126.4.1493
  125. Tsegaye Y, Shintani DK, DellaPenna D (2002) Overexpression of the enzyme p-hydroxyphenolpyruvate dioxygenase in Arabidopsis and its relation to tocopherol biosynthesis. Plant Physiol Biochem 40:913-920 https://doi.org/10.1016/S0981-9428(02)01461-4
  126. Tzin V, Galili G (2010) New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol Plant 3:956-972 https://doi.org/10.1093/mp/ssq048
  127. Tzin V, Malitsky S, Aharoni A, Galili G (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 60:156-167 https://doi.org/10.1111/j.1365-313X.2009.03945.x
  128. Tzin V, Malitsky S, Ben Zvi MM, Bedair M, Sumner L, Aharoni A, Galili G (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 Phytologist 194:430-439 https://doi.org/10.1111/j.1469-8137.2012.04052.x
  129. Tzin V, Rogachev I, Meir S, Ben Zvi MM, Masci T, Vainstein A, Aharoni A, Galili G (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 64:4441-4452 https://doi.org/10.1093/jxb/ert250
  130. Waller JC, Akhtar TA, Lara-Nunez A, Gregory JF 3rd, McQuinn RP, Giovannoni JJ, Hanson AD (2010) Developmental and feed forward control of the expression of folate biosynthesis genes in tomato fruit. Mol Plant 3:66-77 https://doi.org/10.1093/mp/ssp057
  131. Wang W, Xia H , Yang X, Xu T, Si HJ, Cai XX, Wang F, Su J, Snow AA, Lu BB (2014) A novel 5-enolpyruvoylshikimate- 3-phosphate (EPSP) synthase transgene for glyphosate resistance stimulates growth and fecundity in weedy rice (Oryza sativa) without herbicide. New Phytologist 202:679-688 https://doi.org/10.1111/nph.12428
  132. Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee BS, Kaufman LS (2006) G-protein-coupled receptor 1, G-protein G$\alpha$- subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiol 140:844-855 https://doi.org/10.1104/pp.105.071282
  133. Watanabe S, Hayashi K, Yagi K, Asai T, MacTavish H, Picone J, Turnbull C, Watanabe N (2002) Biogenesis of 2-phenylethanol in rose flowers: incorporation of [$^2H_8$]L-phenylalanine into 2-phenylethanol and its $\beta$-D-glucopyranoside during the flower opening of Rosa 'Hoh-Jun' and Rosa damascena Mill. Biosci Biotechno Biochem 66:943-947 https://doi.org/10.1271/bbb.66.943
  134. Wildermuth M, Dewdney J, Wu G, Ausubel F (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature 414:562-565 https://doi.org/10.1038/35107108
  135. Wu J, Woodard RW (2006) New insights into the evolutionary links relating to the 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase subfamilies. J Biol Chem 281:4042-4048 https://doi.org/10.1074/jbc.M512223200
  136. Yamada T, Matsuda F, Kasai K, Fukuoka S, Kitamura K, Tozawa Y, Miyagawa H, Wakasa K (2008) Mutation of a rice gene encoding a phenylalanine biosynthetic enzyme results in accumulation of phenylalanine and tryptophan. Plant Cell 20:1316-1329 https://doi.org/10.1105/tpc.107.057455
  137. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19:2470-2483 https://doi.org/10.1105/tpc.107.050708
  138. Yoo H, Widhalm JR, Qian YC, Maeda H, Cooper BR, Jannasch AS, Gonda I, Lewinsohn E, Rhodes D, Dudareva N (2013) An alternative pathway contributes to phenylalanine biosynthesis in plants via a cytosolic tyrosine: phenylpyruvate aminotransferase. Nat Commun 4:28-33
  139. Zamir LO, Tiberio R, Fiske M, Berry A, Jensen RA (1985) Enzymatic and nonenzymatic dehydration reactions of L-arogenate. Biochemistry 24:1607-1612 https://doi.org/10.1021/bi00328a006
  140. Zhang XH, Brotherton JE, Widholm JM, Portis AR (2001) Targeting a nuclear anthranilate synthase $\alpha$-subunit gene to the tobacco plastid genome results in enhanced tryptophan biosynthesis: return of a gene to its pre-endosymbiotic origin. Plant Physiol 127:131-141 https://doi.org/10.1104/pp.127.1.131
  141. Zhao J, Last RL (1995) Immunological characterization and chloroplast localization of the tryptophan biosynthetic enzymes of the flowering plant Arabidopsis thaliana. J Biol Cheam 270:6081-6087 https://doi.org/10.1074/jbc.270.11.6081