Natural hypolignification is associated with extensive oligolignol accumulation in flax stems

Plant Physiology

Volumn 158, Issue 4, 2012, Pages 1893-1915

  Huis, Rudy ^a,b   Morreel, Kris ^c,d   Fliniaux, Ophélie ^e   Lucau Danila, Anca ^a,b   Fénart, Stéphane ^a,b   Grec, Sébastien ^a,b   Neutelings, Godfrey ^a,b   Chabbert, Brigitte ^f,g   Mesnard, François ^e   Boerjan, Wout ^c,d   Hawkins, Simon ^a,b  

^a UNIV LILLE   (France)

^b Université de Lille 1 Sciences et Technologies   (France)

^c Vlaams Instituut voor Biotechnologie   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

^e UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^f UMR614 FARE   (France)

^g UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYOPHYTA; LINUM USITATISSIMUM;

EID: 84859338182     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.192328     Document Type: Article

References (83)

1. Attoumbré J, Bienaimé C, Dubois F, Fliniaux M-A, Chabbert B, Baltora-Rosset S (2010) Development of antibodies against secoisolariciresinol: application to the immunolocalization of lignans in Linum usitatissimum seeds. Phytochemistry 71: 1979-1987
2. Beejmohun V, Fliniaux O, Grand É, Lamblin F, Bensaddek L, Christen P, Kovensky J, Fliniaux M-A, Mesnard F (2007) Microwave-assisted extraction of the main phenolic compounds in flaxseed. Phytochem Anal 18: 275-282
3. Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Cézard L, Le Bris P, Borrega N, Hervé J, Blondet E, Balzergue S, et al (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23: 1124-1137
4. BoerjanW, Ralph J, BaucherM(2003) Lignin biosynthesis. Annu Rev Plant Biol 54: 519-546
5. Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17: 2281-2295
6. Charlet S, Bensaddek L, Raynaud S, Gillet F, Mesnard F, Fliniaux M-A (2002) An HPLC procedure for the quantification of anhydrosecoisolariciresinol: application to the evaluation of flax lignan content. Plant Physiol Biochem 40: 225-229
7. Charlton A, Donarski J, HarrisonM, Jones S, Godward J, Oehlschlager S, Arques J, Ambrose M, Chinoy C, Mullineaux P, et al (2008) Responses of the pea (Pisum sativum L.) leaf metabolome to drought stress assessed by nuclear magnetic resonance spectroscopy. Metabolomics 4: 312-327
8. Chen SX, Schopfer P (1999) Hydroxyl-radical production in physiological reactions: a novel function of peroxidase. Eur J Biochem 260: 726-735
9. Cloutier S, Ragupathy R, Niu Z, Duguid S (2010) SSR-based linkage map of flax (Linum usitatissimum L.) and mapping of QTLs underlying fatty acid composition traits. Mol Breed 28: 437-451
10. Dauwe R, Morreel K, Goeminne G, Gielen B, Rohde A, Van Beeumen J, Ralph J, Boudet A-M, Kopka J, Rochange SF, et al (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J 52: 263-285
11. Davidson RM, Reeves PA, Manosalva PM, Leach JE (2009) Germins: a diverse protein family important for crop improvement. Plant Sci 177: 499-510
12. Davin LB, Lewis NG (2003) An historical perspective on lignan biosynthesis: monolignol, allyphenol and hydroxycinnamic acid coupling and downstream metabolism. Phytochem Rev 7: 257-288
13. Day A, AddiM, KimW, DavidH, Bert F, Mesnage P, Rolando C, Chabbert B, Neutelings G, Hawkins S (2005a) ESTs from the fibre-bearing stem tissues of flax (Linum usitatissimum L.): expression analyses of sequences related to cell wall development. Plant Biol 7: 23-32
14. Day A, Ruel K, Neutelings G, Crônier D, David H, Hawkins S, Chabbert B (2005b) Lignification in the flax stem: evidence for an unusual lignin in bast fibers. Planta 222: 234-245
15. del Río JC, Rencoret J, Gutiérrez A, Nieto L, Jiménez-Barbero J, Martínez AT (2011) Structural characterization of guaiacyl-rich lignins in flax (Linum usitatissimum) fibers and shives. J Agric Food Chem 59: 11088-11099
16. Demura T, Fukuda H (2007) Transcriptional regulation in wood formation. Trends Plant Sci 12: 64-70
17. De Pauw MA, Vidmar JJ, Collins J, Bennett RA, Deyholos MK (2007) Microarray analysis of bast fibre producing tissues of Cannabis sativa identifies transcripts associated with conserved and specialised processes of secondary cell wall development. Funct Plant Biol 34: 737-749
18. Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics 11: 150
19. Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis IF, Zhuang J, Kaneda M, Mansfield SD, Samuels L, et al (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
20. Faix O (1991) Classification of lignins from different botanical origins by FT-IR spectroscopy. Holzforschung 45: 21-27
21. Fénart S, Ndong Y-P, Duarte J, Rivière N, Wilmer J, van Wuytswinkel O, Lucau A, Cariou E, Neutelings G, Gutierrez L, et al (2010) Development and validation of a flax (Linum usitatissimum L.) gene expression oligo microarray. BMC Genomics 11: 592
22. Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres J-L, Rovira P, Puigdomènech P, et al (2010) ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J 64: 633-644
23. Fornalé S, Sonbol FM, Maes T, Capellades M, Puigdomènech P, Rigau J, Caparrós-Ruiz D (2006) Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors. Plant Mol Biol 62: 809-823
24. Gang DR, Kasahara H, Xia Z-Q, VanderMijnsbrugge K, Bauw G, Boerjan W, Van Montagu M, Davin LB, Lewis NG (1999) Evolution of plant defense mechanisms: relationships of phenylcoumaran benzylic ether reductases to pinoresinol-lariciresinol and isoflavone reductases. J Biol Chem 274: 7516-7527
25. Gorshkova T, Morvan C (2006) Secondary cell-wall assembly in flax phloem fibres: role of galactans. Planta 223: 149-158
26. Hano C, Addi M, Bensaddek L, Crônier D, Baltora-Rosset S, Doussot J, Maury S, Mesnard F, Chabbert B, Hawkins S, et al (2006a) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223: 975-989
27. Hano C, Martin I, Fliniaux O, Legrand B, Gutierrez L, Arroo RR, Mesnard F, Lamblin F, Lainé E (2006b) Pinoresinol-lariciresinol reductase gene expression and secoisolariciresinol diglucoside accumulation in developing flax (Linum usitatissimum) seeds. Planta 224: 1291-1301
28. Hemmati S, von Heimendahl CB, Klaes M, Alfermann AW, Schmidt TJ, Fuss E (2010) Pinoresinol-lariciresinol reductases with opposite enantiospecificity determine the enantiomeric composition of lignans in the different organs of Linum usitatissimum L. Planta Med 76: 928-934
29. Holmborn B, Eckerman C, Eklund P, Hemming J, Nisula L, Reunanen M, Sjöholm R, Sundberg A, Sundberg K, Willför S (2003) Knots in trees: a new rich source of lignans. Phytochem Rev 2: 331-340
30. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
31. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19: 6150-6161
32. Kacurakova M, Capek P, Sasinkova V, Wellner N, Ebringerova A (2000) FT-IR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohydr Polym 43: 195-203
33. Kaneda M, Schuetz M, Lin BSP, Chanis C, Hamberger B, Western TL, Ehlting J, Samuels AL (2011) ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport. J Exp Bot 62: 2063-2077
34. Ko J-H, Prassinos C, Han K-H (2006) Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytol 169: 469-478
35. Kvavadze E, Bar-Yosef O, Belfer-Cohen A, Boaretto E, Jakeli N, Matskevich Z, Meshveliani T (2009) 30,000-year-old wild flax fibers. Science 325: 1359-1359
36. Kwon M, Davin LB, Lewis NG (2001) In situ hybridization and immunolocalization of lignan reductases in woody tissues: implications for heartwood formation and other forms of vascular tissue preservation. Phytochemistry 57: 899-914
37. Lapierre C, Monties B, Rolando C, Chirale L (1985) Thioacidolysis of lignin: comparison with acidolysis. J Wood Chem Technol 5: 277-292
38. Legay S, Sivadon P, Blervacq A-S, Pavy N, Baghdady A, Tremblay L, Levasseur C, Ladouce N, Lapierre C, Séguin A, et al (2010) EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188: 774-786
39. Leplé JC, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, Naumann A, Kang KY, Kim H, Ruel K, et al (2007) Downregulation of cinnamoylcoenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19: 3669-3691
40. Lu F, Ralph J (2003) Non-degradative dissolution and acetylation of ballmilled plant cell walls: high-resolution solution-state NMR. Plant J 35: 535-544
41. Marechal Y, Chanzy H (2000) The hydrogen bond network in Ibeta cellulose as observed by infrared spectrometry. J Mol Struct 523: 183-196
42. McDougall GJ (1992) Changes in cell wall-associated peroxidases during the lignification of flax fibres. Phytochemistry 31: 3385-3389
43. Miao YC, Liu CJ (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
44. Morreel K, Dima O, Kim H, Lu F, Niculaes C, Vanholme R, Dauwe R, Goeminne G, Inzé D, Messens E, et al (2010a) Mass spectrometrybased sequencing of lignin oligomers. Plant Physiol 153: 1464-1478
45. Morreel K, Kim H, Lu F, Dima O, Akiyama T, Vanholme R, Niculaes C, Goeminne G, Inzé D, Messens E, et al (2010b) Mass spectrometrybased fragmentation as an identification tool in lignomics. Anal Chem 82: 8095-8105
46. Morreel K, Ralph J, Kim H, Lu F, Goeminne G, Ralph S, Messens E, Boerjan W (2004) Profiling of oligolignols reveals monolignol coupling conditions in lignifying poplar xylem. Plant Physiol 136: 3537-3549
47. Moss G (2000) Nomenclature of lignans and neolignans. Pure Appl Chem 72: 1493-1523
48. Niedźwiedź-Siegień I (1998) Cyanogenic glucosides in Linum usitatissimum. Phytochemistry 49: 59-63
49. Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9: 534-540
50. Paux E, Tamasloukht M, Ladouce N, Sivadon P, Grima-Pettenati J (2004) Identification of genes preferentially expressed during wood formation in Eucalyptus. Plant Mol Biol 55: 263-280
51. Prassinos C, Ko JH, Yang J, Han KH (2005) Transcriptome profiling of vertical stem segments provides insights into the genetic regulation of secondary growth in hybrid aspen trees. Plant Cell Physiol 46: 1213-1225
52. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61-76
53. Qin YM, Hu CY, Zhu YX (2008) The ascorbate peroxidase regulated by H(2) O(2) and ethylene is involved in cotton fiber cell elongation by modulating ROS homeostasis. Plant Signal Behav 3: 194-196
54. Ragupathy R, Rathinavelu R, Cloutier S (2011) Physical mapping and BAC-end sequence analysis provide initial insights into the flax (Linum usitatissimum L.) genome. BMC Genomics 12: 217
55. Ralph J, Akiyama T, KimH, Lu F, Schatz PF, Marita JM, Ralph SA, Reddy MS, Chen F, Dixon RA (2006) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J Biol Chem 281: 8843-8853
56. Ramires EC, Megiatto JD Jr, Gardrat C, Castellan A, Frollini E (2010) Valorization of an industrial organosolv-sugarcane bagasse lignin: characterization and use as a matrix in biobased composites reinforced with sisal fibers. Biotechnol Bioeng 107: 612-621
57. Ros Barcelo A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207: 207-216
58. Shadle G, Chen F, Srinivasa Reddy MS, Jackson L, Nakashima J, Dixon RA (2007) Down-regulation of hydroxycinnamoyl CoA:shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochemistry 68: 1521-1529
59. Singh KK, Mridula D, Rehal J, Barnwal P (2011) Flaxseed: a potential source of food, feed and fiber. Crit Rev Food Sci Nutr 51: 210-222
60. Sterjiades R, Dean JFD, Gamble G, Himmelsbach DS, Eriksson K-EL (1993) Extracellular laccases and peroxidases from sycamore maple (Acer pseudoplatanus) cell-suspension cultures. Planta 190: 75-87
61. Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH, et al (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101: 13951-13956
62. Struijs K, Vincken JP, Doeswijk TG, Voragen AG, Gruppen H (2009) The chain length of lignan macromolecule from flaxseed hulls is determined by the incorporation of coumaric acid glucosides and ferulic acid glucosides. Phytochemistry 70: 262-269
63. Summerscales J, Dissanayake N, Virk AS, Hall W (2010) A review of bast fibres and their composites: I. Fibres as reinforcements. Compos Part A Appl Sci Manuf 41: 1329-1335
64. Syrjanen K, Brunow G (1998) Oxidative cross coupling of p-hydroxycinnamic alcohols with dimeric arylglycerol b-aryl ether lignin model compounds: the effect of oxidation potentials. J Chem Soc Perkin Trans 1: 3425-3430
65. Toure A, Xu XM (2010) Flaxseed lignans: source, biosynthesis, metabolism, antioxidant activity, bio-active components, and health benefits. Compr Rev Food Sci Food Saf 9: 261-269
66. Touzel JP, Chabbert B, Monties B, Debeire P, Cathala B (2003) Synthesis and characterization of dehydrogenation polymers in Gluconacetobacter xylinus cellulose and cellulose/pectin composite. J Agric Food Chem 51: 981-986
67. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121
68. van den Broeck HC, Maliepaard C, Ebskamp MJM, Toonen MAJ, Koops AJ (2008) Differential expression of genes involved in C1 metabolism and lignin biosynthesis in wooden core and bast tissues of fibre hemp (Cannabis sativa L.). Plant Sci 174: 205-220
69. Vander Mijnsbrugge K, Beeckman H, De Rycke R, Van Montagu M, Engler G, BoerjanW(2000) Phenylcoumaran benzylic ether reductase, a prominent poplar xylem protein, is strongly associated with phenylpropanoid biosynthesis in lignifying cells. Planta 211: 502-509
70. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11: 278-285
71. Vanholme R, Ralph J, Akiyama T, Lu FC, Pazo JR, Kim H, Christensen JH, Van Reusel B, Storme V, De Rycke R, et al (2010) Engineering traditional monolignols out of lignin by concomitant up-regulation of F5H1 and down-regulation of COMT in Arabidopsis. Plant J 64: 885-897
72. Venglat P, Xiang D, Qiu S, Stone SL, Tibiche C, Cram D, Alting-Mees M, Nowak J, Cloutier S, DeyholosM, et al (2011) Gene expression analysis of flax seed development. BMC Plant Biol 11: 74
73. Wagner A, Ralph J, Akiyama T, Flint H, Phillips L, Torr K, Nanayakkara B, Te Kiri L (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA:shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc Natl Acad Sci USA 104: 11856-11861
74. Weng J-K, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187: 273-285
75. Westcott N, Muir A (2003) Flax seed lignan in disease prevention and health promotion. Phytochem Rev 2: 401-417
76. Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Cell 7: 1001-1013
77. Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22: 1249-1263
78. Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580: 1183-1191
79. Zhang J, Elo A, Helariutta Y (2011) Arabidopsis as a model for wood formation. Curr Opin Biotechnol 22: 293-299
80. Zhao C, Avci U, Grant EH, Haigler CH, Beers EP (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53: 425-436
81. Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16: 227-233
82. Zhong R, Lee C, Ye Z-H (2010) Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci 15: 625-632
83. Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21: 248-266