Coniferyl alcohol hinders the growth of tobacco BY-2 cells and Nicotiana benthamiana seedlings

Planta

Volumn 242, Issue 3, 2015, Pages 747-760

  Väisänen, Enni E ^a   Smeds, Annika I ^b   Fagerstedt, Kurt V ^a   Teeri, Teemu H ^a   Willför, Stefan M ^b   Kärkönen, Anna ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Coniferyl alcohol; Lignification; Monolignol metabolism; Monolignol toxicity; Potassium iodide

Indexed keywords

NICOTIANA BENTHAMIANA; NICOTIANA TABACUM;

CONIFERYL ALCOHOL; PHENOL DERIVATIVE;

CYTOLOGY; DRUG EFFECTS; SEEDLING; TOBACCO;

PHENOLS; SEEDLINGS; TOBACCO;

EID: 84939470881     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2348-7     Document Type: Article

References (55)

1. Alejandro S, Lee Y, Tohge T, Sudre D, Osorio S, Park J, Bovet L, Lee Y, Geldner N, Fernie AR, Martinoia E (2012) AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol 22:1207–1212
2. Amelot N, Carrouche A, Danoun S, Bourque S, Haiech J, Pugin A, Ranjeva R, Grima-Pettenati J, Mazars C, Briere C (2011) Cryptogein, a fungal elicitor, remodels the phenylpropanoid metabolism of tobacco cell suspension cultures in a calcium-dependent manner. Plant, Cell Environ 34:149–161
3. Bassard J-E, Richert L, Geerinck J, Renault H, Duval F, Ullmann P, Schmitt M, Meyer E, Mutterer J, Boerjan W, De Jaeger D, Mely Y, Goossens A, Werck-Reichhart D (2012) Protein-protein and protein-membrane associations in the lignin pathway. Plant Cell 24:4465–4482
4. Beejmohun V, Fliniaux O, Hano C, Pilard S, Grand E, Lesur D, Cailleu D, Lamblin F, Lainé E, Kovensky J, Fliniaux MA, Mesnard F (2007) Coniferin dimerisation in lignan biosynthesis in flax cells. Phytochemistry 68:2744–2752
5. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546
6. Boija E, Johansson G (2006) Interactions between model membranes and lignin-related compounds studied by immobilized liposome chromatography. Biochim Biophys Acta 1758:620–626
7. Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363
8. Borges da Silva EA, Zabkova M, Araújo JD, Cateto CA, Barreiro MF, Belgacem MN, Rodrigues AE (2009) An integrated process to produce vanillin and lignin-based polyurethanes from Kraft lignin. Chem Eng Res Des 87:1276–1292
9. Calvo-Flores FG, Dobado JA (2010) Lignin as renewable raw material. Chem Sus Chem 3:1227–1235
10. Cong F, Diehl BG, Hill JL, Brown NR, Tien M (2013) Covalent bond formation between amino acids and lignin: cross-coupling between proteins and lignin. Phytochemistry 96:449–456
11. Daurade-Le Vagueresse MH, Romiti C, Grosclaude C, Bounias M (2001) Coevolutionary toxicity as suggested by differential coniferyl alcohol inhibition of Ceratocystis species growth. Toxicon 39:203–208
12. Dima O, Morreel K, Vanholme B, Kim H, Ralph J, Boerjan W (2015) Small glycosylated lignin oligomers are stored in Arabidopsis leaf vacuoles. Plant Cell 27:695–710
13. dos Santos WD, Ferrarese MLL, Nakamura CV, Mourão KSM, Mangolin CA, Ferrarese-Filho O (2008) Soybean (Glycine max) root lignification induced by ferulic acid. The possible mode of action. J Chem Ecol 34:1230–1241
14. Fagerstedt KV, Kukkola EM, Koistinen VVT, Takahashi J, Marjamaa K (2010) Cell wall lignin is polymerised by class III secretable plant peroxidases in Norway spruce. J Integr Plant Biol 52:186–194
15. Freudenberg K, Harkin JM (1963) The glucosides of cambial sap of spruce. Phytochemistry 2:189–193
16. Gachon CMM, Langlois-Meurinne M, Saindrenan P (2005) Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci 10:542–549
17. Hosokawa M, Suzuki S, Umezawa T, Sato Y (2001) Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol 42:959–968
18. Huwiler M, Bürgi U, Kohler H (1985) Mechanism of enzymatic and non-enzymatic tyrosine iodation. Inhibition by excess hydrogen peroxide and/or iodide. Eur J Biochem 147:469–476
19. Kaneda M, Rensing KH, Wong JCT, Banno B, Mansfield SD, Samuels AL (2008) Tracking monolignols during wood development in lodgepole pine. Plant Physiol 147:1750–1760
20. Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32
21. Kärkönen A, Koutaniemi S, Mustonen M, Syrjänen K, Brunow G, Kilpeläinen I, Teeri TH, Simola LK (2002) Lignification related enzymes in Picea abies suspension cultures. Physiol Plant 114:343–353
22. Kim H, Ralph J, Lu F, Pilate G, Leplé J-C, Pollet B, Lapierre C (2002) Identification of the structure and origin of thioacidolysis marker compounds for cinnamyl alcohol dehydrogenase deficiency in angiosperms. J Biol Chem 277:47412–47419
23. König S, Feussner K, Kaever A, Landesfeind M, Thurow C, Karlovsky P, Gatz C, Polle A, Feussner I (2014) Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytol 202:823–837
24. Lee S, Monnappa AK, Mitchell RJ (2012) Biological activities of lignin hydrolysate-related compounds. BMB Rep 45:265–274
25. Leinhos V, Savidge RA (1993) Isolation of protoplastsfrom developing xylem of Pinus banksiana and Pinus strobus. Can J Forest Res 23:343–348
26. Li Z-H, Wang Q, Ruan X, Pan C-D, Jiang D-A (2010) Phenolics and plant allelopathy. Molecules 15:8933–8952
27. Miao Y-C, Liu C-J (2010) ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc Natl Acad Sci USA 107:22728–22733
28. Milder IEJ, Arts ICW, Venema DP, Lasaroms JJP, Vähälä K, Hollman PCH (2004) Optimization of a liquid chromatography—tandem mass spectrometry method for quantification of the plant lignans secoisolariciresinol, matairesinol, lariciresinol, and pinoresinol in foods. J Agr Food Chem 52:4643–4651
29. Morikawa Y, Yoshinaga A, Kamitakahara H, Wada M, Takabe K (2010) Cellular distribution of coniferin in differentiating xylem of Chamaecyparis obtusa as revealed by Raman microscopy. Holzforschung 64:61–67
30. Müller K, Linkies A, Vreeburg RAM, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150:1855–1865
31. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
32. Muscolo A, Panuccio MR, Sidari M (2001) The effect of phenols on respiratory enzymes in seed germination. Respiratory enzyme activities during germination of Pinus laricio seeds treated with phenols extracted from different forest soils. Plant Growth Regul 35:31–35
33. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants. Int Rev Cytol 132:1–30
34. Nair RB, Bastress KL, Ruegger MO, Denault JW, Chapple C (2004) The Arabidopsis thalianaREDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell 16:544–554
35. Nakashima J, Awano T, Takabe K, Fujita M, Saiki H (1997) Immunocytochemical localization of phenylalanine ammonia-lyase and cinnamyl alcohol dehydrogenase in differentiating tracheary elements derived from Zinnia mesophyll cells. Plant Cell Physiol 38:113–123
36. Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci USA 109:10101–10106
37. Nose M, Bernards MA, Furlan M, Zajicek J, Eberhardt TL, Lewis NG (1995) Towards the specification of consecutive steps in macromolecular lignin assembly. Phytochemistry 39:71–79
38. Önnerud H, Zhang L, Gellerstedt G, Henriksson G (2002) Polymerization of monolignols by redox shuttle—mediated enzymatic oxidation: a new model in lignin biosynthesis I. Plant Cell 14:1953–1962
39. Pesquet E, Zhang B, Gorzsás A, Puhakainen T, Serk H, Escamez S, Barbier O, Gerber L, Courtois-Moreau C, Alatalo E, Paulin L, Kangasjärvi J, Sundberg B, Goffner D, Tuominen H (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25:1314–1328
40. Pomar F, Merino F, Ros Barceló A (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol-HCl) reaction. Protoplasma 220:17–28
41. Ralph J, MacKay JJ, Hatfield RD, O’Malley DM, Whetten RW, Sederoff RR (1997) Abnormal lignin in a loblolly pine mutant. Science 277:235–239
42. Ro DK, Mah N, Ellis BE, Douglas CJ (2001) Functional characterization and subcellular localization of poplar (Populus trichocarpa x Populus deltoides) cinnamate 4-hydroxylase. Plant Physiol 126:317–329
43. Savidge RA, Förster H (2001) Coniferyl alcohol metabolism in conifers-II. Coniferyl alcohol and dihydroconiferyl alcohol biosynthesis. Phytochemistry 57:1095–1103
44. Smeds AI, Eklund PC, Sjöholm RE, Willför SM, Nishibe S, Deyama T, Holmbom BR (2007) Quantification of a broad spectrum of lignans in cereals, oilseeds, and nuts. J Agr Food Chem 55:1337–1346
45. Smeds AI, Eklund PC, Monogioudi E, Willför SM (2012) Chemical characterization of polymerized products formed in the reactions of matairesinol and pinoresinol with the stable radical 2,2-diphenyl-1-picrylhydrazyl. Holzforschung 66:283–294
46. Smith RA, Schuetz M, Roach M, Mansfield SD, Ellis B, Samuels L (2013) Neighboring parenchyma cells contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous. Plant Cell 25:3988–3999
47. Syrjänen K, Brunow G (2000) Regioselectivity in lignin biosynthesis. The influence of dimerization and cross-coupling. J Chem Soc Perk T 1:183–187
48. Tobimatsu Y, Wagner A, Donaldson L, Mitra P, Niculaes C, Dima O, Kim JI, Anderson N, Loque D, Boerjan W, Chapple C, Ralph J (2013) Visualization of plant cell wall lignification using fluorescence-tagged monolignols. Plant J 76:357–366
49. Tsuyama T, Kawai R, Shitan N, Matoh T, Sugiyama J, Yoshinaga A, Takabe K, Fujita M, Yazaki K (2013) Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiol 162:918–926
50. Wang Y, Chantreau M, Sibout R, Hawkins S (2013) Plant cell wall lignification and monolignol metabolism. Front Plant Sci 4:220. doi:10.3389/fpls.2013.00220
51. Weir TL, Park S-W, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479
52. Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Cell 7:1001–1013
53. Winkel-Shirley B (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol Plant 107:142–149
54. Wyrambik D, Grisebach H (1975) Purification and properties of isoenzymes of cinnamyl-alcohol dehydrogenase from soybean-cell-suspension cultures. Eur J Biochem 59:9–15
55. Zhang K, Bhuiya M-W, Pazo JR, Miao Y, Kim H, Ralph J, Liu CJ (2012) An engineered monolignol 4-O-methyltransferase depresses lignin biosynthesis and confers novel metabolic capability in Arabidopsis. Plant Cell 24:3135–3152