Redirection of metabolite biosynthesis from hydroxybenzoates to volatile terpenoids in green hairy roots of Daucus carota

Planta

Volumn 243, Issue 2, 2016, Pages 305-320

  Mukherjee, Chiranjit ^a   Samanta, Tanmoy ^a   Mitra, Adinpunya ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY   (India)

Author keywords

1 deoxy d xylulose 5 phosphate reductoisomerase (DXR); Daucus; Green hairy roots; Isoprenoid; Methyl erythritol 4 phosphate (MEP); p Hydroxybenzoic acid; Phenylpropanoid; Volatile terpenoid

Indexed keywords

ALCOHOL DEHYDROGENASE; CHLOROPHYLL; HYDROGEN PEROXIDE; HYDROXYBENZOIC ACID DERIVATIVE; ISOMERASE; PHENOLIC ACID; PLANT PROTEIN; PYRUVATE KINASE; SHIKIMATE DEHYDROGENASE; TERPENE;

CARROT; CHEMISTRY; MASS FRAGMENTOGRAPHY; METABOLISM; PLANT ROOT;

ALCOHOL OXIDOREDUCTASES; CHLOROPHYLL; DAUCUS CAROTA; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HYDROGEN PEROXIDE; HYDROXYBENZOATES; ISOMERASES; METABOLIC NETWORKS AND PATHWAYS; PLANT PROTEINS; PLANT ROOTS; PYRUVATE KINASE; TERPENES;

EID: 84955332487     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2403-4     Document Type: Article

References (67)

1. Alasalvar C, Grigor JM, Zhang D, Quantick PC, Shahidi F (2001) Composition of volatiles, phenolics, sugars, antioxidant vitamins and sensory quality of different coloured carrot varieties. J Agric Food Chem 49:1410–1416
2. Andre C, Benning C (2007) Arabidopsis seedlings deficient in a plastidic pyruvate kinase are unable to utilize seed storage compounds for germination and establishment. Plant Physiol 145:1670–1680
3. Ap Rees T, Hill SA (1994) Metabolic control analysis of plant metabolism. Plant Cell Environ 17:587–599
4. Asuming WA, Beauchamp PS, Descalzo JT, Dev BC, Dev V, Frost S, Ma CW (2005) Essential oil composition of four Lomatium Raf. species and their chemotaxonomy. Biochem Syst Ecol 33:17–26
5. Banerjee A, Sharkey T (2014) Methylerythritol 4-phosphate (MEP) pathway metabolic regulation. Nat Prod Rep 31:1043–1055
6. Behnke K, Kaiser A, Zimmer I, Brüggemann N, Janz D, Polle A, Hampp R, Hänsch R, Popko J, Schmitt-Kopplin P, Ehlting B, Rennenberg H, Barta C, Loreto F, Schnitzler J (2010) RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Mol Biol 74:61–75
7. Bera P, Samanta T, Kotamreddy JNR, Mitra A (2015) Inter-specific variation in headspace scent volatiles composition of four commercially-cultivated jasmine flowers. Nat Prod Res 29:1328–1335
8. Bergmeyer HU, Gawehn K, Grassl M (1974) Enzymatic assay of pyruvate kinase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 2nd edn. Academic Press, New York, pp 509–510
9. Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:1151–1154
10. Carretero-Paulet L, Ahumada I, Cunillera N, Rodríguez-Concepción M, Ferrer A, Boronat A, Campos N (2002) Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-d-erythritol 4-phosphate pathway. Plant Physiol 129:1581–1591
11. Chakraborty D, Sircar D, Mitra A (2008) Phenylalanine ammonia-lyase-mediated biosynthesis of 2-hydroxy-4-methoxybenzaldehyde in roots of Hemidesmus indicus. J Plant Physiol 165:1033–1040
12. da Silva MHL, Andrade EHA, Zoghbi MGB, Luz AIR, da Silva JD, Maia JGS (1999) The essential oils of Lantana camara L. occurring in North Brazil. Flavour Frag J 14:208–210
13. Daferera DL, Ziogas BN, Polissiou MG (2003) The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Prot 22:39–44
14. Díaz J, Barceló R, de Caceres FMA (1997) Changes in shikimate dehydrogenase and the end products of the shikimate pathway, chlorogenic acid and lignins, during the early development of seedlings of Capsicum annum. New Phytol 136:183–188
15. Fell DA (1992) Metabolic control analysis: a survey of its theoretical and experimental development. Biochem J 286:313–330
16. Flores HE, Doi Y, Cuello JL, Maldonado-Mendoza IE, Loyola-Vargas VM (1993) Green roots: photosynthesis and photoautotrophy in an underground plant organ. Plant Physiol 101:363–371
17. Flores-Pérez Û, Pérez-Gil J, Closa M, Wright LP, Botella-Pavía P, Phillips MA, Ferrer A, Gershenzon J, Rodríguez-Concepción M (2010) PLEIOTROPIC REGULATORY LOCUS 1 (PRL1) integrates the regulation of sugar responses with isoprenoid metabolism in Arabidopsis. Mol Plant 3:101–112
18. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265
19. Gaid MM, Sircar D, Beuerle T, Mitra A, Beerhues L (2009) Benzaldehyde dehydrogenase from chitosan-treated Sorbus aucuparia cell cultures. J Plant Physiol 166:1343–1349
20. Gaid MM, Sircar D, Müller A, Beuerle T, Liu B, Ernst L, Hänsch R, Beerhues L (2012) Cinnamate: CoA ligase initiates the biosynthesis of a benzoate-derived xanthone phytoalexin in Hypericum calycinum cell cultures. Plant Physiol 160:1267–1280
21. Ge X, d’Avignon DA, Ackerman JH, Sammons RD (2012) Observation and identification of 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate in horseweed and ryegrass treated with glyphosate. Pestic Biochem Physiol 104:187–191
22. Guerra D, Anderson AJ, Salisbury FB (1985) Reduced phenylalanine ammonia-lyase and tyrosine ammonia-lyase activities and lignin synthesis in wheat grown under low pressure sodium lamps. Plant Physiol 78:126–130
23. Haderlie HC, Widholm JM, Slife FW (1977) Effect of glyphosate on carrot and tobacco cells. Plant Physiol 60:40–43
24. Hall DO, Rao KK (1994) Photosynthesis, 5th edn. Cambridge University Press, Cambridge, pp 39–51
25. Hamill JD, Parr AJ, Rhodes MJC, Robins RJ, Walton NJ (1987) New routes to plant secondary products. Biotechnology 5:800–804
26. Hampel D, Mosandl A, Wüst M (2005) Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66:305–311
27. Hartley RD, Harris PJ (1981) Phenolic constituents of cell walls of dicotyledonous. Biochem Syst Ecol 9:198–203
28. Hemm MR, Rider SD, Ogas J, Murry DJ, Chapple C (2004) Light induces phenylpropanoid metabolism in Arabidopsis roots. Plant J 38:765–778
29. Herrmann KM (1995) The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7:907–919
30. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184
31. Jacob A, Malpathak N (2004) Green hairy cultures of Solanum khasianum Clarke—a new route to in vitro solasodine production. Curr Sci 87:1442–1447
32. Kang YH, Parker CC, Smith AC, Waldron KW (2008) Characterization and distribution of phenolics in carrot cell wall. J Agric Food Chem 56:8558–8564
33. Kjeldsen F, Christensen LP, Edelenbos M (2001) Quantitative analysis of aroma compounds in carrot (Daucus carota L.) cultivars by capillary gas chromatography using large-volume injection technique. J Agric Food Chem 49:4342–4348
34. Kundu A, Jawali N, Mitra A (2012) Shikimate pathway modulates the elicitor-stimulated accumulation of fragment 2-hydroxy-4-methoxybenzaldehyde in Hemidesmus indicus root. Plant Physiol Biochem 56:104–108
35. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
36. Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264:14486–14492
37. Lorato F, Ciccioli P, Brancaleoni E, Cecinato A, Frattoni M, Sharkey TD (1996) Different sources of reduced carbon contribute to form three classes of terpenoid emitted by Quercus ilex L. leaves. Proc Natl Acad Sci USA 93:9966–9969
38. Loreto F, Schnitzler J (2010) Abiotic stress and induced BVOCs. Trends Plant Sci 15:156–166
39. Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787
40. Mahmoud SS, Croteau RB (2001) Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA 98:8915–8920
41. Maiti S, Moon UR, Bera P, Samanta T, Mitra A (2014) The in vitro antioxidant capacities of Polianthes tuberosa L. flower extracts. Acta Physiol Plant 36:2597–2605
42. Mitra A, Mayer MJ, Mellon FA, Michael AJ, Narbad A, Parr AJ, Waldron K, Walton NJ (2002) 4-Hydroxycinnamoyl-CoA-hydratase/lyase, an enzyme of phenylpropanoid cleavage from Pseudomonas, causes formation of C6–C1 glucose conjugates when expressed in hairy roots of Datura stramonium. Planta 15:79–89
43. 31P-NMR spectroscopy after specific inhibition of 2-C-methyl-d-erythritol 2,4-cyclodiphosphate reductase. Effect of light and temperature. Plant, Cell Environ 34:1241–1247
44. Mukherjee C, Sircar D, Chatterjee M, Das S, Mitra A (2014) Combating photooxidative stress in green hairy roots of Daucus carota cultivated under light irradiation. J Plant Physiol 171:179–187
45. Nishida K (1963) Osmotic swelling of isolated chloroplast. Plant Cell Physiol 4:247–256
46. Qually AV, Widhalm JR, Adebesin F, Kish CM, Dudareva N (2012) Completion of the core β-oxidative pathway of benzoic acid biosynthesis in plants. Proc Natl Acad Sci USA 109:16383–16388
47. Ramak P, Osaloo SK, Ebrahimzadeh H, Sharifi M, Behmanesh M (2013) Inhibition of the mevalonate pathway enhances carvacrol biosynthesis and DXR gene expression in shoot cultures of Satureja khuzistanica Jamzad. J Plant Physiol 170:1187–1193
48. Rhodes MJC, Parr AJ, Walton NJ (1997) Studies of secondary metabolic pathways in transformed roots. In: Doran PM (ed) Hairy roots: culture and applications. Harwood Academic Publishers, Amsterdam, pp 31–41
49. Rivasseau C, Seemann M, Boisson AM, Streb P, Gout E, Douce R, Rohmer M, Bligny R (2009) Accumulation of 2-C-methyl-d-erythritol 2,4-cyclodiphosphate in illuminated plant leaves at supraoptimal temperatures reveals a bottleneck of the prokaryotic methylerythritol 4-phosphate pathway of isoprenoid biosynthesis. Plant Cell Environ 32:82–92
50. Rodríguez-Concepción M, Boronat A (2015) Breaking new grounds in the regulation of early steps of plant isoprenoid biosynthesis. Curr Opin Plant Biol 25:17–22
51. Rohmer M (1999) The discovery of a mevalonate independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 16:565–574
52. Ross JR, Nam KH, D’Auria JC, Pichersky E (1999) S-Adenosyl-l-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys 367:9–16
53. Schnitzler JP, Madlung J, Rose A, Seitz HU (1992) Biosynthesis of p-hydroxybenzoic acid in elicitor treated carrot cell cultures. Planta 188:594–600
54. Sircar D, Mitra A (2008) Evidence for p-hydroxybenzoate formation involving phenylpropanoid chain-cleavage in hairy roots of Daucus carota. J Plant Physiol 165:407–414
55. Sircar D, Mitra A (2009) Accumulation of p-hydroxybenzoic acid in hairy roots of Daucus carota 2. Confirming biosynthetic steps through feeding of inhibitors and precursors. J Plant Physiol 166:1370–1380
56. Sircar D, Roychowdhury A, Mitra A (2007a) Accumulation of p-hydroxybenzoic acid in hairy roots of Daucus carota. J Plant Physiol 164:1358–1366
57. Sircar D, Dey G, Mitra A (2007b) A validated HPLC method for simultaneous determination of 2-hydroxy-4-methoxybenzaldehyde and 2-hydroxy-4-methoxybenzoic acid in root organs of Hemidesmus indicus. Chromatographia 65:349–353
58. Sircar D, Mukherjee C, Beuerle T, Beerhues L, Mitra A (2011) Characterization of p-hydroxybenzaldehyde dehydrogenase, the final enzyme of p-hydroxybenzoic acid biosynthesis in hairy roots of Daucus carota. Acta Physiol Plant 33:2019–3024
59. Sircar A, Cardoso HG, Mukherjee C, Mitra A, Arnholdt-Schmitt B (2012) Alternative oxidase (AOX) and phenolic metabolism in methyl-jasmonate treated hairy root cultures of Daucus carota L. J Plant Physiol 169:657–663
60. Souret FF, Weathers PJ, Wobbe KK (2002) The mevalonate-independent pathway is expressed in transformed roots of Artemisia annua and regulated by light and culture age. In Vitro Cell Dev Biol Plant 38:581–588
61. Taya M, Sato H, Kino-Oka M, Tone S (1994) Characterization of Pak-Bung green hairy roots cultivated under light irradiation. J Ferment Bioeng 78:42–48
62. Tone S, Taya M, Kino-Oka M (1997) Alteration of metabolite formation and morphological properties of hairy roots by environmental stimuli. In: Doran PM (ed) Hairy roots: culture and applications. Harwood Academic Publishers, Amsterdam, pp 65–72
63. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291
64. Vollsnes AV, Melø TB, Futsaether CM (2012) Photomorphogenesis and pigment induction in lentil seedling roots exposed to low light conditions. Plant Biol 14:467–474
65. Wildermuth MC (2006) Variation on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296
66. Wright LP, Rohwer JM, Ghirardo A, Hammerbacher A, Ortiz-Alcaide M, Raguschke B, Schnitzler J-P, Gershenzon J, Phillips MA (2014) Deoxyxylulose 5-phosphate synthase controls flux through the methylerythritol 4-phosphate pathway in Arabidopsis. Plant Physiol 165:1488–1504
67. Zeng S, Liu Y, Wang Y (2013) Light stress suppresses the accumulation of epimedins A, B, C, and icariin in Epimedium, a traditional medicinal plant. Acta Physiol Plant 35:3271–3275