Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin polymers in seed coats

Plant Cell

Volumn 25, Issue 7, 2013, Pages 2587-2600

  Tobimatsu, Yuki ^a   Chen, Fang ^b,c,e   Nakashima, Jin ^b   Escamilla Treviño, Luis L ^b,c,e   Jackson, Lisa ^b,c   Dixon, Richard A ^b,c,e   Ralph, John ^a,d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b PLANT BIOLOGY DIVISION   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d USA   (United States)

^e UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLEOMACEAE; CLEOME HASSLERIANA; DICOTYLEDONEAE; EUPHORBIACEAE;

LIGNIN; METHYLTRANSFERASE; POLYMER;

ANGIOSPERM; ARTICLE; BIOSYNTHESIS; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; CLEOME; CONFOCAL MICROSCOPY; ENZYMOLOGY; EUPHORBIACEAE; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT; PLANT SEED; SPECIES DIFFERENCE;

ANGIOSPERMS; BIOSYNTHETIC PATHWAYS; CELL WALL; CLEOME; EUPHORBIACEAE; LIGNIN; MAGNETIC RESONANCE SPECTROSCOPY; METHYLTRANSFERASES; MICROSCOPY, CONFOCAL; MOLECULAR STRUCTURE; PLANTS; POLYMERS; SEEDS; SPECIES SPECIFICITY;

EID: 84883150515     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.113142     Document Type: Article

References (71)

1. Abdulla, R., Chan, E.S., and Ravindra, P. (2011). Biodiesel production from Jatropha curcas: A critical review. Crit. Rev. Biotechnol. 31: 53-64.
2. Albersheim, P., Nevins, D.J., English, P.D., and Karr, A. (1967). A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr. Res. 5: 340-345.
3. Arsovski, A.A., Haughn, G.W., and Western, T.L. (2010). Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signal. Behav. 5: 796-801.
4. Bewley, J.D., Bradford, K., Hilhorst, H.M., and Nonogaki, H. (2013). Structure and Composition. In Seeds, J.D. Bewley, K. Bradford, H.M. Hilhorst, and H. Nonogaki, eds (New York: Springer), pp. 1-25.
5. Björkman, A. (1954). Isolation of lignin from finely divided wood with neutral solvents. Nature 174: 1057-1058.
6. Boerjan, W., Ralph, J., and Baucher, M. (2003). Lignin biosynthesis. Annu. Rev. Plant Biol. 54: 519-546.
7. Bonawitz, N.D., and Chapple, C. (2010). The genetics of lignin biosynthesis: Connecting genotype to phenotype. Annu. Rev. Genet. 44: 337-363.
8. Bonawitz, N.D., and Chapple, C. (2013). Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty? Curr. Opin. Biotechnol. 24: 336-343.
9. Carpita, N.C. (2012). Progress in the biological synthesis of the plant cell wall: New ideas for improving biomass for bioenergy. Curr. Opin. Biotechnol. 23: 330-337.
10. Cathala, B., Saake, B., Faix, O., and Monties, B. (2003). Association behaviour of lignins and lignin model compounds studied by multidetector size-exclusion chromatography. J. Chromatogr. A 1020: 229-239.
11. Chen, F., and Dixon, R.A. (2007). Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25: 759-761.
12. Chen, F., Kota, P., Blount, J.W., and Dixon, R.A. (2001). Chemical syntheses of caffeoyl and 5-OH coniferyl aldehydes and alcohols and determination of lignin O-methyltransferase activities in dicot and monocot species. Phytochemistry 58: 1035-1042.
13. Chen, F., Tobimatsu, Y., Havkin-Frenkel, D., Dixon, R.A., and Ralph, J. (2012). A polymer of caffeyl alcohol in plant seeds. Proc. Natl. Acad. Sci. USA 109: 1772-1777.
14. Chen, F., Tobimatsu, Y., Jackson, L., Nakashima, J., Ralph, J., and Dixon, R.A. (2013). Novel seed coat lignins in the Cactaceae: Structure, distribution and implications for the evolution of lignin diversity. Plant J. 73: 201-211.
15. Debeaujon, I., Lepiniec, L., Pourcel, L., and Routaboul, J.M. (2007). Seed coat development and dormancy. In Annual Plant Reviews: Seed Development, Dormancy and Germination, Vol. 27, K.J. Bradford and H. Nonogaki, eds (Oxford, U.K.: Blackwell Publishing, Inc.) pp. 25-49.
16. Dixon, R.A., Xie, D.Y., and Sharma, S.B. (2005). Proanthocyanidins-A final frontier in flavonoid research? New Phytol. 165: 9-28.
17. Egley, G.H., Paul, R.N., Vaughn, K.C., and Duke, S.O. (1983). Role of peroxidase in the development of water-impermeable seed coats in Sida spinosa L. Planta 157: 224-232.
18. Elumalai, S., Tobimatsu, Y., Grabber, J.H., Pan, X., and Ralph, J. (2012). Epigallocatechin gallate incorporation into lignin enhances the alkaline delignification and enzymatic saccharification of cell walls. Biotechnol. Biofuels 5: 59.
19. Faix, O., Lange, W., and Besold, G. (1981). Molecular-weight determinations of DHPs from mixtures of precursors by steric exclusion chromatography (HPLC). Holzforschung 35: 137-140.
20. Hatfield, R.D., Jung, H.G., Ralph, J., Buxton, D.R., and Weimer, P.J. (1994). A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures. J. Sci. Food Agric. 65: 51-58.
21. Haughn, G., and Chaudhury, A. (2005). Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10: 472-477.
22. Holtman, K.M., Chang, H.M., and Kadla, J.F. (2007). An NMR comparison of the whole lignin from milled wood, MWL, and REL dissolved by the DMSO/NMI procedure. J. Wood Chem. Technol. 27: 179-200.
23. Kao, Y.Y., Harding, S.A., and Tsai, C.J. (2002). Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol. 130: 796-807.
24. Kelly, K.M., Vanstaden, J., and Bell, W.E. (1992). Seed coat structure and dormancy. Plant Growth Regul. 11: 201-209.
25. Klein, A.P., Beach, E.S., Emerson, J.W., and Zimmerman, J.B. (2010). Accelerated solvent extraction of lignin from Aleurites moluccana (Candlenut) nutshells. J. Agric. Food Chem. 58: 10045-10048.
26. Lapierre, C., Monties, B., and Rolando, C. (1985). Thioacidolysis of lignin: Comparison with acidolysis. J. Wood Chem. Technol. 5: 277-292.
27. Lapierre, C., Monties, B., and Rolando, C. (1986). Thioacidolysis of poplar lignins: Identification of monomeric syringyl products and characterization of guaiacyl-syringyl lignin fractions. Holzforschung 40: 113-118.
28. Lepiniec, L., Debeaujon, I., Routaboul, J.M., Baudry, A., Pourcel, L., Nesi, N., and Caboche, M. (2006). Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57: 405-430.
29. Liang, M.X., Davis, E., Gardner, D., Cai, X.N., and Wu, Y.J. (2006). Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224: 1185-1196.
30. Lu, F., Marita, J.M., Lapierre, C., Jouanin, L., Morreel, K., Boerjan, W., and Ralph, J. (2010). Sequencing around 5-hydroxyconiferyl alcohol-derived units in caffeic acid O-methyltransferase-deficient poplar lignins. Plant Physiol. 153: 569-579.
31. Lu, F., and Ralph, J. (2003). Non-degradative dissolution and acetylation of ball-milled plant cell walls: High-resolution solution-state NMR. Plant J. 35: 535-544.
32. Mansfield, S.D. (2009). Solutions for dissolution-Engineering cell walls for deconstruction. Curr. Opin. Biotechnol. 20: 286-294.
33. Mansfield, S.D., Kim, H., Lu, F., and Ralph, J. (2012). Whole plant cell wall characterization using solution-state 2D NMR. Nat. Protoc. 7: 1579-1589.
34. Marita, J.M., Ralph, J., Hatfield, R.D., Guo, D., Chen, F., and Dixon, R.A. (2003). Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase. Phytochemistry 62: 53-65.
35. Marita, J.M., Ralph, J., Lapierre, C., Jouanin, L., and Boerjan, W. (2001). NMR characterization of lignins from transgenic poplars with suppressed caffeic acid O-methyltransferase activity. J. Chem. Soc., Perkin Trans. 2939-2945.
36. Martin, C., Moure, A., Martin, G., Carrillo, E., Dominguez, H., and Parajo, J.C. (2010). Fractional characterisation of jatropha, neem, moringa, trisperma, castor and candlenut seeds as potential feedstocks for biodiesel production in Cuba. Biomass Bioenergy 34: 533-538.
37. Moinuddin, S.G.A., Jourdes, M., Laskar, D.D., Ki, C., Cardenas, C.L., Kim, K.-W., Zhang, D., Davin, L.B., and Lewis, N.G. (2010). Insights into lignin primary structure and deconstruction from Arabidopsis thaliana COMT (caffeic acid O-methyl transferase) mutant Atomt1. Org. Biomol. Chem. 8: 3928-3946.
38. Morreel, K., Ralph, J., Lu, F., Goeminne, G., Busson, R., Herdewijn, P., Goeman, J.L., Van der Eycken, J., Boerjan, W., and Messens, E. (2004). Phenolic profiling of caffeic acid O-methyltransferasedeficient poplar reveals novel benzodioxane oligolignols. Plant Physiol. 136: 4023-4036.
39. North, H., et al. (2010). Arabidopsis seed secrets unravelled after a decade of genetic and omics-driven research. Plant J. 61: 971-981.
40. Pesquet, E., et al. (2013). Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25: 1314-1328.
41. Ralph, J., Akiyama, T., Kim, H., Lu, F., Schatz, P.F., Marita, J.M., Ralph, S.A., Reddy, M.S.S., Chen, F., and Dixon, R.A. (2006). Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J. Biol. Chem. 281: 8843-8853.
42. Ralph, J., Lapierre, C., Lu, F., Marita, J.M., Pilate, G., Van Doorsselaere, J., Boerjan, W., and Jouanin, L. (2001a). NMR evidence for benzodioxane structures resulting from incorporation of 5-hydroxyconiferyl alcohol into lignins of O-methyltransferasedeficient poplars. J. Agric. Food Chem. 49: 86-91.
43. Ralph, J., et al. (2001b). Elucidation of new structures in lignins of CAD-and COMT-deficient plants by NMR. Phytochemistry 57: 993-1003.
44. Reeve, R.M. (1959a). Histological and histochemical changes in developing and ripening peaches. III. Cate-chol tannin content per cell. Am. J. Bot. 46: 645-650.
45. Reeve, R.M. (1959b). Histological and histochemical changes in developing and ripening peaches. I. The catechol tannins. Am. J. Bot. 46: 210-217.
46. Rencoret, J., Ralph, J., Marques, G., Gutiérrez, A., Martínez, Á.T., and Del Río, J.C. (2013). Structural characterization of the lignin from coconut (Cocos nucifera) coir fibers. J. Agric. Food Chem. 61: 2434-2445.
47. Rolston, M.P. (1978). Water impermeable seed dormancy. Bot. Rev. 44: 365-396.
48. Selvendran, R.R., and O'Neill, M.A. (1987). Isolation and analysis of cell walls from plant material. Methods Biochem. Anal. 32: 25-153.
49. Simmons, B.A., Loqué, D., and Ralph, J. (2010). Advances in modifying lignin for enhanced biofuel production. Curr. Opin. Plant Biol. 13: 313-320.
50. Stewart, J.J., Akiyama, T., Chapple, C.C.S., Ralph, J., and Mansfield, S.D. (2009). The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol. 150: 621-635.
51. Stöckigt, J., and Zenk, M.H. (1975). Chemical syntheses and properties of hydroxycinnamoyl-coenzyme A derivatives. Z. Naturforsch., C, Biosci. 30: 352-358.
52. Sujatha, M., Reddy, T.P., and Mahasi, M.J. (2008). Role of biotechnological interventions in the improvement of castor (Ricinus communis L.) and Jatropha curcas L. Biotechnol. Adv. 26: 424-435.
53. Tobimatsu, Y., Davidson, C.L., Grabber, J.H., and Ralph, J. (2011). Fluorescence-tagged monolignols: Synthesis, and application to studying in vitro lignification. Biomacromolecules 12: 1752-1761.
54. Tobimatsu, Y., Elumalai, S., Grabber, J.H., Davidson, C.L., Pan, X., and Ralph, J. (2012). Hydroxycinnamate conjugates as potential monolignol replacements: In vitro lignification and cell wall studies with rosmarinic acid. ChemSusChem 5: 676-686.
55. Tobimatsu, Y., Takano, T., Kamitakahara, H., and Nakatsubo, F. (2006). Studies on the dehydrogenative polymerizations of monolignol beta-glycosides. Part 2: Horseradish peroxidase catalyzed dehydrogenative polymerization of isoconiferin. Holzforschung 60: 513-518.
56. Umezawa, T. (2010). The cinnamate/monolignol pathway. Phytochem. Rev. 9: 1-17.
57. Updegraff, D.M. (1969). Semi micro determination of cellulose in biological materials. Anal. Biochem. 32: 420-424.
58. Vanholme, R., Demedts, B., Morreel, K., Ralph, J., and Boerjan, W. (2010a). Lignin biosynthesis and structure. Plant Physiol. 153: 895-905.
59. Vanholme, R., Morreel, K., Darrah, C., Oyarce, P., Grabber, J.H., Ralph, J., and Boerjan, W. (2012). Metabolic engineering of novel lignin in biomass crops. New Phytol. 196: 978-1000.
60. Vanholme, R., Morreel, K., Ralph, J., and Boerjan, W. (2008). Lignin engineering. Curr. Opin. Plant Biol. 11: 278-285.
61. Vanholme, R., Ralph, J., Akiyama, T., Lu, F., Rencoret Pazo, J., Christensen, J., Rohde, A., Morreel, K., DeRycke, R., Kim, H., Van Reusel, B., and Boerjan, W. (2010b). Engineering traditional monolignols out of lignins by concomitant up-regulation F5H1 and down-regulation of COMT in Arabidopsis. Plant J. 64: 885-897.
62. Vega-Sánchez, M.E., and Ronald, P.C. (2010). Genetic and biotechnological approaches for biofuel crop improvement. Curr. Opin. Biotechnol. 21: 218-224.
63. Vogt, T. (2010). Phenylpropanoid biosynthesis. Mol. Plant 3: 2-20.
64. Wagner, A., Tobimatsu, Y., Phillips, L., Flint, H., Torr, K.M., Donaldson, L., Pears, L., and Ralph, J. (2011). CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant J. 67: 119-129.
65. Watanabe, T., Shino, A., Akashi, K., and Kikuchi, J. (2012). Spectroscopic investigation of tissue-specific biomass profiling for Jatropha curcas L. Plant Biotechnol. 29: 163-170.
66. Weng, J.K., and Chapple, C. (2010). The origin and evolution of lignin biosynthesis. New Phytol. 187: 273-285.
67. Weng, J.K., Li, X., Bonawitz, N.D., and Chapple, C. (2008). Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr. Opin. Biotechnol. 19: 166-172.
68. Weng, J.-K., Mo, H., and Chapple, C. (2010). Over-expression of F5H in COMT-deficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation. Plant J. 64: 898-911.
69. Wever, D.A.Z., Heeres, H.J., and Broekhuis, A.A. (2012). Characterization of Physic nut (Jatropha curcas L.) shells. Biomass Bioenergy 37: 177-187.
70. Yamamura, M., Akashi, K., Yokota, A., Hattori, T., Suzuki, S., Shibata, D., and Umezawa, T. (2012). Characterization of Jatropha curcas lignins. Plant Biotechnol. 29: 179-183.
71. Yue, F., Lu, F., Sun, R., andRalph, J. (2012). Synthesis and characterization of new 5-linked pinoresinol lignin models. Chemistry 18: 16402-16410.