The cell biology of lignification in higher plants

Annals of Botany

Volumn 115, Issue 7, 2015, Pages 1053-1074

  Barros, Jaime ^a,b   Serk, Henrik ^a   Granlund, Irene ^a,c   Pesquet, Edouard ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF NORTH TEXAS   (United States)

^c C/o Umea Biotech Incubator AB ^*  (Sweden)

Author keywords

Arabidopsis thaliana; laccases; lignification; Lignin; monolignols; non cell autonomous processes; peroxidases; plant cell wall

Indexed keywords

CELLS AND CELL COMPONENTS; DICOTYLEDON; ENZYME ACTIVITY; LIGNIN; METABOLISM; PHENOTYPE;

ARABIDOPSIS THALIANA; EMBRYOPHYTA;

LIGNIN;

ARABIDOPSIS; CELL WALL; EMBRYOPHYTA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ARABIDOPSIS; CELL WALL; EMBRYOPHYTA; GENE EXPRESSION REGULATION, PLANT; LIGNIN;

EID: 84930467649     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcv046     Document Type: Review

References (230)

1. Achnine DL, Blancaflor EB, Rasmussen S, Dixon RA. 2004. Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. The Plant Cell 16: 3098-3109.
2. Adler E. 1977. Lignin chemistry-past, present and future. Wood Science and Technology 3: 169-218.
3. Alejandro S, Lee Y, Tohge T, et al. 2012. AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Current Biology 22: 1207-1212.
4. Bao W, O'Malley DM, Whetten R, Sederoff RR. 1993. A laccase associated with lignification in loblolly pine xylem. Science 260: 672-674.
5. Bassard JE, Richert L, Geerinck J, et al. 2012. Protein-protein and protein-membrane associations in the lignin pathway. The Plant Cell 24: 4465-4482.
6. Bell-Lelong DA, Cusumano JC, Meyer K, Chapple C. 1997. Cinnamate-4-hydroxylase expression in Arabidopsis (regulation in response to development and the environment). Plant Physiology 113: 729-738.
7. Berthet S, Demont-Caulet N, Pollet B, et al. 2011. Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. The Plant Cell 23: 1124-1137.
8. Bewley JD. 1997. Breaking down the walls-a role for endo-P-mannanase in release from seed dormancy? Trends in Plant Science 2: 464-469.
9. Blanco-Portales R, Medina-Escobar N, Lopez-Raez JA, et al. 2002. Cloning, expression and immunolocalization pattern of a cinnamyl alcohol dehydrogenase gene from strawberry (Fragaria x ananassa cv. Chandler). Journal of Experimental Botany 53: 1723-1734.
10. Blee KA, Choi JW, O'Connell AP, Schuch W, Lewis NG, Bolwell GP. 2003. A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry 64: 163-176.
11. Blodgett JT, Herms DA, Bonello P. 2005. Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. Forest Ecology and Management 208:373-3 82.
12. Blokhina OB, Chirkova TV, Fagerstedt KV. 2001. Anoxic stress leads to hydrogen peroxide formation in plant cells. Journal of Experimental Botany 52: 1179-1190.
13. Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology, 54: 519-546.
14. Boija E, Johansson G. 2006. Interactions between model membranes and lig-nin-related compounds studied by immobilized liposome chromatography. Biochimica et Biophysica Acta 1758: 620-626.
15. Boija E, Lundquist A, Edwards K, Johansson G. 2007. Evaluation of bilayer disks as plant cell membrane models in partition studies. Analytical Biochemistry 364: 145-152.
16. Bonawitz ND, Chapple C. 2010. The genetics of lignin biosynthesis: connecting genotype to phenotype. Annual Review of Genetics 44: 337-363
17. Bonawitz ND, Kim JI, Tobimatsu Y, et al. 2014. Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 509: 376-380.
18. Brown DM, Leo AHZ, 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. The Plant Cell 17: 2281-2295.
19. Brunow G, Lundquist K. 1980. Comparison of a synthetic dehydrogenation polymer of coniferyl alcohol with milled wood lignin from spruce, using 1H NMR spectroscopy. Paperija Puu 62: 669-672.
20. Cabane M, Pireaux JC, Leger E, et al. 2004. Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiology 134: 586-594.
21. Cahill DM, McComb JA. 1992. A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) andE. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 40: 315-332.
22. Cai C, Xu C, Li X, Ferguson I, Chen K. 2006. Accumulation of lignin in relation to change in activities of lignification enzymes in loquat fruit flesh after harvest. Postharvest Biology and Technology 40: 163-169.
23. Caparros-Ruiz D, Fornale S, Civardi L, Puigdomenech P, Rigau J. 2006. Isolation and characterisation of a family of laccases in maize. Plant Science 171: 217-225.
24. Capellades M, Torres MA, Bastisch I, et al. 1996. The maize caffeic acid O-methyltransferase gene promoter is active in transgenic tobacco and maize plant tissues. Plant Molecular Biology 31: 307-322.
25. Chaffey N, Barlow P, Sundberg B. 2002. Understanding the role of the cyto-skeleton in wood formation in angiosperm trees: hybrid aspen (Populus tremulaxP. tremuloides) as the model species. Tree Physiology 22: 239-249.
26. Chapelle A, Morreel K, Vanholme R, et al. 2012. Impact of the absence of stem-specific P-glucosidases on lignin and monolignols. Plant Physiology 160: 1204-1217.
27. Chen CH, Meyermans H, Burggraeve B, et al. 2000. Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant Physiology 123: 853-868.
28. Chen F, Tobimatsu Y, Havkin-Frenkel D, Dixon RA, Ralph J. 2012. A polymer of caffeyl alcohol in plant seeds. Proceedings of the National Academy of Sciences, USA 109: 1772-1777.
29. Chen F, Tobimatsu Y, Jackson L, Nakashima J, Ralph J, Dixon RA. 2013. Novel seed coat lignins in the Cactaceae: structure, distribution and implications for the evolution of lignin diversity. The Plant Journal 73: 201-211.
30. Chen HC, Li Q, Shuford CM, et al. 2011. Membrane protein complexes catalyze both 4-and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis. Proceedings of the National Academy of Sciences, USA 108: 21253-21258.
31. Coy MR, Salem TZ, Denton JS, et al. 2010. Phenol-oxidizing laccases from the termite gut. Insect Biochemistry and Molecular Biology 40: 723-732.
32. Crestini C, Crucianelli M, Orlandi M, Saladino R. 2010. Oxidative strategies in lignin chemistry: a new environmental friendly approach for the function-alisation of lignin and lignocellulosic fibers. Catalysis Today 156: 8-22.
33. D'Autréaux B, Toledano MB. 2007. ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Nature Reviews Molecular Cell Biology 8: 813-824.
34. 2 on the vasculature and phenolic secondary metabolism of Plantago maritima. Phytochemistry 65: 2197-2204.
35. Davin LB, Lewis NG. 1992. Phenylpropanoid metabolism: biosynthesis of monolignols, lignans and neolignans, lignins and suberins. In: HA Stafford, RK, Ibrahim, eds. Phenolic metabolism in plants. New York: Springer: 325-375.
36. Davin LB, Lewis NG. 2000. Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiology 123: 453-462.
37. Dean JF, Eriksson KEL. 1994. Laccase and the deposition of lignin in vascular plants. Holzforschung-International Journal of the Biology, Chemistry, Physics and Technology of Wood 48: 21-33.
38. Dean JF, LaFayette PR, Rugh C, et al. 1998. Laccases associated with lignify-ing vascular tissues. ACS Symposium Series 697: 96-108.
39. Debeaujon I, Lepiniec L, Pourcel L, Routaboul JM. 2007. Seed coat development and dormancy. Seed development, dormancy and germination. Annual Plant Reviews 27: 25-49.
40. Delessert C, Wilson I, Van Der Straeten D, Dennis E, Dolferus R. 2004. Spatial and temporal analysis of the local response to wounding. Plant Molecular Biology 55: 165-181.
41. Del Río JC, Rencoret J, Prinsen P, Martínez AT, Ralph J, Gutiérrez A. 2012. Structural characterization of wheat straw lignin as revealed by analytical pyrolysis, 2D-NMR, and reductive cleavage methods. Journal of Agricultural and Food Chemistry 60: 5922-5935.
42. Demont-Caulet N, Lapierre C, Jouanin L, Baumberger S, Méchin V. 2010. Arabidopsis peroxidase-catalyzed copolymerization of coniferyl and sinapyl alcohols: kinetics of an endwise process. Phytochemistry 71: 1673-1683.
43. De Pinto MC, Ros Barceló A. 1997. Cytochemical localization of phenol-oxiding enzymes in lignifying Coleus blumei stems. European Journal of Histochemistry 41: 17-22.
44. Do CT, Pollet B, Thévenin L, et al. 2007. Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 226: 1117-1129.
45. Donaldson LA. 2001. Lignification and lignin topochemistry-an ultrastructural view. Phytochemistry 57: 859-873.
46. Donaldson LA, Singh AP, Yoshinaga A, Takabe K. 1999. Lignin distribution in mild compression wood of Pinus radiata. Canadian Journal of Botany 77: 41-50.
47. Dwivedi UN, Singh P, Pandey VP, Kumar A. 2011. Structure-function relationship among bacterial, fungal and plant laccases. Journal of Molecular Catalysis B: Enzymatic 68: 117-128.
48. Ek M, Gellerstedt G, and Henriksson G. 2009. Lignin In: G Henriksson, ed. Pulp and paper chemistry and technology, Volume 1: Wood chemistry and biotechnology. Walter de Gruyter GmbH & Co. KG, 121-124.
49. El Kayal W, Keller G, Debayles C, et al. 2006. Regulation of tocopherol biosynthesis through transcriptional control of tocopherol cyclase during cold hardening in Eucalyptus gunnii. Physiologia Plantarum 126: 212-223.
50. Fagerstedt KV, Kukkola EM, Koistinen VV, Takahashi J, Marjamaa K. 2010. Cell wall lignin is polymerised by class III secretable plant peroxidases in Norway spruce. Journal of Integrative Plant Biology 52: 186-194.
51. Fan L, Linker R, Gepstein S, Tanimoto E, Yamamoto R, Neumann PM. 2006. Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lig-nin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiology 140: 603-612.
52. Fernández-Pérez F, Pomar F, Pedreño MA, Novo-Uzal E. 2014. The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units. Physiologia Plantarum (in press).
53. Fernández-Pérez F, Vivar T, Pomar F, Pedreño MA, Novo-Uzal E. 2015. Peroxidase 4 is involved in syringyl lignin formation in Arabidopsis thali-ana. Journal of Plant Physiology 175: 86-94.
54. Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC, Chapple C. 2000. Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. The Plant Journal 22: 223-234.
55. Fromm J, Rockel B, Lautner S, Windeisen E, Wanner G. 2003. Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques. Journal of Structural Biology 143: 77-84.
56. Fujita M, Harada H. 1979. Autoradiographic investigations of cell wall development. II. Tritiated phenylalanine and ferulic acid assimilation in relation to lignification. Mokuzai Gakkaishi 25: 89-94.
57. Fukuda H. 1997. Tracheary element differentiation. The Plant Cell 9: 1147.
58. Gansert D. 2003. Xylem sap flow as a major pathway for oxygen supply to the sapwood of birch (Betula pubescens Eh.). Plant, Cell and Environment 26: 1803-1814.
59. Gavnholt B, Larsen K. 2002. Molecular biology of plant laccases in relation to lignin formation. Physiologia Plantarum 116: 273-280.
60. Geldner N. 2013. The endodermis. Annual Review of Plant Biology 64: 531-558.
61. Gibson LJ. 2012. The hierarchical structure and mechanics of plant materials. Journal of the Royal Society Interface 9: 2749-2766.
62. Gierlinger N. 2014. Revealing changes in molecular composition of plant cell walls on the micron-level by Raman mapping and vertex component analysis (VCA). Frontiers in Plant Science 5: 306.
63. Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48: 909-930.
64. Gorzsás A, Stenlund H, Persson P, Trygg J, Sundberg B. 2011. Cell-specific chemotyping and multivariate imaging by combined FT-IR microspectro-scopy and orthogonal projections to latent structures (OPLS) analysis reveals the chemical landscape of secondary xylem. The Plant Journal 66: 903-914.
65. Goujon T, Sibout R, Pollet B, et al. 2003. A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sina-poyl esters. Plant Molecular Biology 51: 973-989.
66. Grabber JH, Schatz PF, Kim H, Lu F, Ralph J. 2010. Identifying new lignin bioengineering targets: 1. Monolignol-substitute impacts on lignin formation and cell wall fermentability. BMC Plant Biology, 10: 114.
67. Gray-Mitsumune M, Molitor EK, Cukovic D, Carlson JE, Douglas CJ. 1999. Developmentally regulated patterns of expression directed by poplar PAL promoters in transgenic tobacco and poplar. Plant Molecular Biology 39: 657-669.
68. Guerra A, Ferraz A, Cotrim AR, da Silva FT. 2000. Polymerization of lignin fragments contained in a model effluent by polyphenoloxidases and horseradish peroxidase/hydrogen peroxide system. Enzyme and Microbial Technology 26: 315-323.
69. Gui J, Shen J, Li L. 2011. Functional characterization of evolutionarily divergent 4-coumarate: coenzyme A ligases in rice. Plant Physiology 157: 574-586.
70. Guo D, Chen F, Dixon RA. 2002. Monolignol biosynthesis in microsomal preparations from lignifying stems of alfalfa (Medicago sativa L.). Phytochemistry 61: 657-667.
71. Halls SC, Lewis NG. 2002. Secondary and quaternary structures of the ()-pinoresinol-forming dirigent protein. Biochemistry 41: 9455-9461.
72. Hano C, Addi M, Bensaddek L, et al. 2006. Differential accumulation of mono-lignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223: 975-989.
73. Harding SA, Leshkevich J, Chiang VL, Tsai CJ. 2002. Differential substrate inhibition couples kinetically distinct 4-coumarate:coenzyme A ligases with spatially distinct metabolic roles in quaking aspen. Plant Physiology 128: 428-438.
74. Harkin JM. 1967. Lignin-a natural polymeric product of phenol oxidation. In: WI Taylor, AR Battersby, eds. Oxidative coupling of ohenols, New York: Marcel Dekker, 243-321.
75. Hausman JF, Evers D, Thiellement H, Jouve L. 2000. Compared responses of poplar cuttings and in vitro raised shoots to short-term chilling treatments. Plant Cell Reports 19: 954-960.
76. Hawkins S, Boudet A. 2003. Defence lignin and hydroxycinnamyl alcohol dehydrogenase activities in wounded Eucalyptus gunnii. Forest Pathology 33: 91-104.
77. Hepler PK, Fosket DE, Newcomb EH. 1970. Lignification during secondary wall formation in Coleus: an electron microscopic study. American Journal of Botany 57: 85-96.
78. Herbette S, Bouchet B, Brunel N, Bonnin E, Cochard H, Guillon F. 2015. Immunolabelling of intervessel pits for polysaccharides and lignin helps in understanding their hydraulic properties in Populus tremula x alba. Annals ofBotrany 115: 187-199.
79. Herrero J, Fernandez-Perez F, Yebra T, et al. 2013. Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis. Planta 237: 1599-1612.
80. Higuchi T. 1990. Lignin biochemistry: biosynthesis and biodegradation. Wood Science and Technology 24: 23-63.
81. Higuchi T, Ito Y. 1958. Dehydrogenation products of coniferyl alcohol formed by the action of mushroom phenol oxidase, rhus-laccase and radish peroxidase. Journal of Biochemistry 45: 575-579.
82. Hilal M, Parrado MF, Rosa M, et al. 2004. Epidermal lignin deposition in qui-noa cotyledons in response to UV-B radiation. Photochemistry and Photobiology 79: 205-210.
83. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H. 2001. A large family of class III plant peroxidases. Plant and Cell Physiology, 42:462-468.
84. Hoffmann L, Besseau S, Geoffroy P, et al. 2004. Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyl transferase affects phenylpropanoid biosynthesis. The Plant Cell 16: 1446-1465.
85. Hosmani PS, Kamiya T, Danku J, et al. 2013. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proceedings of the National Academy of Sciences, USA 110: 14498-14503.
86. 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 and Cell Physiology 42: 959-968.
87. Hsieh LS, Ma GJ, Yang CC, Lee PD. 2010. Cloning, expression, site-directed mutagenesis and immunolocalization of phenylalanine ammonia-lyase in Bambusa oldhamii. Phytochemistry 71: 1999-2009.
88. Hu WJ, Kawaoka A, Tsai CJ, et al. 1998. Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proceedings of the National Academy of Sciences, USA95: 5407-5412.
89. Ito Y, Tokunaga N, Sato Y, Fukuda H. 2004. Transfer of phenylpropanoids via the medium between xylem cells in Zinnia xylogenic culture. Plant Biotechnoogy 21: 205-213.
90. Jones L, Ennos AR, Turner SR. 2001. Cloning and characterization of irregular xylem4 (IRX4): a severely lignin-deficient mutant of Arabidopsis. The Plant Journal 26: 205-216.
91. Kaneda M, Rensing KH, Wong JC, Banno B, Mansfield SD, Samuels AL. 2008. Tracking monolignols during wood development in lodgepole pine. Plant Physiology 147: 1750-1760.
92. Karkonen A, Koutaniemi S, Mustonen M, et al. 2002. Lignification related enzymes in Picea abies suspension cultures. Physiologia Plantarum 114: 343-353.
93. Karlsson M, Melzer M, Prokhorenko I, Johansson T, Wingsle G. 2005. Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans. Journal of Experimental Botany 56:2085-2093.
94. Karpinska B, Karlsson M, Schinkel H, et al. 2001. A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization. Plant Physiology 126: 1668-1677.
95. Kawasaki T, Henmi K, Ono E, et al. 1999. The small GTP-binding protein Rac is a regulator of cell death in plants. Proceedings of the National Academy of Sciences, USA 96: 10922-10926.
96. Kawasaki T, Koita H, Nakatsubo T, et al. 2006. Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proceedings of the National Academy of Sciences, USA 103: 230-235.
97. Kelly KM, Van Staden J, Bell WE. 1992. Seed coat structure and dormancy. Plant Growth Regulation 11: 201-209.
98. Kersey R, Inoue K, Schubert KR, Dixon RA. 1999. Immunolocalization of two lignin O-methyltransferases in stems of alfalfa (Medicago sativa L). Protoplasma 209:46-57.
99. Kim YJ, Kim DG, Lee SH, Lee I. 2006. Wound-induced expression of the ferulate 5-hydroxylase gene in Camptotheca acuminata. Biochimica et Biophysica Acta 1760: 182-190.
100. Kotula L, Ranathunge K, Schreiber L, Steudle E. 2009. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. Journal of Experimental Botany 60: 2155-2167.
101. Koutaniemi S, Malmberg HA, Simola LK, Teeri TH, Karkonen A. 2015. Norway spruce (Picea abies) laccases; characterisation of a laccase in a lig-nin-forming tissue culture. Journal ofIntegrative Plant Biology (in press).
102. Kwon M, Burlat V, Davin LB, Lewis NG. 1999. Localization of dirigent protein involved in lignan biosynthesis: implications for lignification at the tissue and subcellular level. In: GG Gross, RW Hemingway, T Yoshida, eds. Plant polyphenols 2: chemistry, biology, pharmacology, ecology. New York: Kluwer Academic Publishers/Plenum Publishers, 393-411.
103. Lacombe E, Hawkins S, Doorsselaere J, et al. 1997. Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. The Plant Journal 11: 429-441.
104. Lagrimini LM, Burkhart W, Moyer M, Rothstein S. 1987. Molecular cloning of complementary DNA encoding the lignin-forming peroxidase from tobacco: molecular analysis and tissue-specific expression. Proceedings of the National Academy of Sciences, USA 84: 7542-7546.
105. Lamport DTA. 1986. Roles for peroxidases in cell wall genesis. In: H Greppin, C Penel, T Gaspar, eds. Molecular and physiological aspects of plant peroxidases. Geneva, Switzerland: Universite de Geneve, 199-208.
106. Lan W, Lu F, Regner M, et al. 2015. Tricin, a flavonoid monomer in monocot lignification. Plant Physiology (in press).
107. Lange BM, Lapierre C, Sandermann H. 1995. Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physiology 108: 1277-1287.
108. Lanot A, Hodge D, Jackson RG, et al. 2006. The glucosyltransferase UGT72E2 is responsible for monolignol 4-O-glucoside production in Arabidopsis thaliana. The Plant Journal 48: 286-295.
109. Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D, Grima-Pettenati J. 2001. Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57: 1187-1195.
110. Lee D, Ellard M, Wanner LA, Davis KR, Douglas CJ. 1995. The Arabidopsis thaliana 4-coumarate: CoA ligase (4CL) gene: stress and developmentally regulated expression and nucleotide sequence of its cDNA. Plant Molecular Biology 28: 871-884.
111. Lee Y, Rubio MC, Alassimone J, Geldner N. 2013. A mechanism for localized lignin deposition in the endodermis. Cell 153:402-412.
112. Li L, Osakabe Y, Joshi CP, Chiang VL. 1999. Secondary xylem-specific expression of caffeoyl-coenzyme A 3-O-methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Molecular Biology 40:555-565.
113. Li L, Cheng XF, Leshkevich J, Umezawa T, Harding SA, Chiang VL. 2001. The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase. The Plant Cell 13: 1567-1586.
114. Li Y, Kajita S, Kawai S, Katayama Y, Morohoshi N. 2003. Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. Journal of Plant Research 116: 175-182.
115. Liang M, Davis E, Gardner D, Cai X, Wu Y. 2006. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224: 1185-1196.
116. 2-~~ in the production of HO-: in vitro and in vivo. Free Radical Biology and Medicine 16: 29-33
117. Liu L, Dean JF, Friedman WE, Eriksson KEL. 1994. A laccase-like pheno-loxidase is correlated with lignin biosynthesis in Zinnia elegans stem tissues. The Plant Journal 6: 213-224.
118. Liu CJ. 2012. Deciphering the enigma of lignification: precursor transport, oxidation, and the topochemistry of lignin assembly. Molecular Plant 5: 304-317.
119. Lu F, Marita JM, Lapierre C, et al. 2010. Sequencing around 5-hydroxyconi-feryl alcohol-derived units in caffeic acid O-methyltransferase-deficient poplar lignins. Plant Physiology 153:569-79.
120. Lu S, Li Q, Wei H, et al. 2013. Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proceedings of the National Academy of Sciences, USA 110: 10848-10853.
121. Lucas WJ, Groover A, Lichtenberger R, et al. 2013. The plant vascular system: evolution, development and functions. Journal of Integrative Plant Biology 55: 294-388.
122. Mäder M, Nessel A, Boff M. 1977. On the physiological significance of the iso-zyme groups of peroxidase from tobacco demonstrated by biochemical properties. Zeitschrift für Pflanzenphysiology 82: 247-260.
123. Mäder M, Ungemach J, Schloß P. 1980. The role of peroxidase isoenzyme groups of Nicotiana tabacum in hydrogen peroxide formation. Planta 147: 467-470.
124. Makkar RS, Tsuneda A, Tokuyasu K, Mori Y. 2001. Lentinula edodes produces a multicomponent protein complex containing manganese (II)-dependent peroxidase, laccase and b-glucosidase. FEMS Microbiology Letters 200: 175-179.
125. Mansfield SD, Kim H, Lu F, Ralph J. 2012. Whole plant cell wall characterization using solution-state 2D NMR. Nature Protocols 7: 1579-1589.
126. Marita JM, Ralph J, Hatfield RD, Guo D, Chen F, Dixon RA. 2003. Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coen-zyme A 3-O-methyltransferase. Phytochemistry 62: 53-65.
127. Martín JA, Solla A, Woodward S, Gil L. 2007. Detection of differential changes in lignin composition of elm xylem tissues inoculated with Ophiostoma novo-ulmi using Fourier transform-infrared spectroscopy. Forest Pathology 37: 187-191.
128. Ménard D, Pesquet E. 2015. Cellular interactions during tracheary elements formation and function. Current Opinion in Plant Biology 23: 109-115.
129. Miao YC, Liu CJ. 2010. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proceedings of the National Academy of Sciences, USA 107: 22728-22733.
130. Min D, Chang H, Jameel H, Lucia L, Wang Z, Jin Y. 2014. The structure of lignin of corn stover and its changes induced by mild sodium hydroxide treatment. BioResources 9: 2405-2414.
131. Mir Derikvand M, Berrio Sierra J, Ruel K, et al. 2008. Redirection of the phe-nylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227: 943-956.
132. Moerschbacher BM, Noll U, Gorrichon L, Reisener HJ. 1990. Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiology 93: 465-470.
133. Moinuddin SG, Jourdes M, Laskar DD, et al. 2010. Insights into lignin primary structure and deconstruction from Arabidopsis thaliana COMT (caf-feic acid O-methyl transferase) mutant Atomt1. Organic and Biomolecular Chemistry 8: 3928-3946.
134. Morreel K, Ralph J, Kim H, et al. 2004. Profiling of oligolignols reveals mono-lignol coupling conditions in lignifying poplar xylem. Plant Physiology 136: 3537-3549.
135. Moura JC, Silva M, Bonine CSV, Viana JOF, Dornelas MC, Mazzafera P. 2010. Abiotic and biotic stresses and changes in the lignin content and composition in plants. Journal of Integrative Plant Biology 52: 360-376.
136. Nair RB, Xia Q, Kartha CJ, et al. 2002. Arabidopsis CYP98A3 mediating aromatic 3-hydroxylation. Developmental regulation of the gene, and expression in yeast. Plant Physiology 130: 210-220.
137. Nakanomyo I, Kost B, Chua NH, Fukuda H. 2002. Preferential and asymmetrical accumulation of a Rac small GTPase mRNA in differentiating xylem cells of Zinnia elegans. Plant and Cell Physiology 43: 1484-1492.
138. 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 and Cell Physiology 38: 113-123.
139. 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. Proceedings of the National Academy of Sciences, USA 109: 10101-10106.
140. Oda Y, Iida Y, Kondo Y, Fukuda H. 2010. Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Current Biology 20: 1197-1202.
141. Ogawa KI, Kanematsu S, Asada K. 1997. Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. Plant and Cell Physiology 38: 1118-1126.
142. Ohl S, Hedrick SA, Chory J, Lamb CJ. 1990. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. The Plant Cell 2: 837-848.
143. Onnerud H, Zhang L, Gellerstedt G, Henriksson G. 2002. Polymerization of monolignols by redox shuttle-mediated enzymatic oxidation: a new model in lignin biosynthesis I. The Plant Cell 14: 1953-1962.
144. Osakabe Y, Nanto K, Kitamura H, et al. 2006. Immunological detection and cellular localization of the phenylalanine ammonia-lyase of a hybrid aspen. Plant Biotechnology 23: 399-404.
145. Østergaard L, Teilum K, Mirza O, et al. 2000. Arabidopsis ATP A2 peroxidase. Expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Molecular Biology 44:231-243.
146. Overmyer K, Tuominen H, Kettunen R, et al. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. The Plant Cell 12: 1849-1862.
147. Passardi F, Penel C, Dunand C. 2004. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends in Plant Science 9: 534-540.
148. Pedreira J, Herrera MT, Zarra I, Revilla G. 2010. The overexpression of AtPrx37, an apoplastic peroxidase, reduces growth in Arabidopsis. Physiologia Plantarum 141:177-87.
149. Pesquet E, Lloyd C. 2011. Microtubules, MAPs and xylem formation. In: B Liu, ed. The plant cytoskeleton. New York: Springer, 277-306.
150. Pesquet E, Korolev AV, Calder G, Lloyd CW. 2010. The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Current Biology 20: 744-749.
151. Pesquet E, Zhang B, Gorzsas A, et al. 2013. Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. The Plant Cell 25: 1314-1328.
152. Petrik DL, Karlen SD, Cass CL, et al. 2013. p-Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon. The Plant Journal 77:713-726.
153. Pickett-Heaps JD, Vanholme R, Cesarino I, et al. 1968. Xylem wall deposition. Protoplasma 65: 181-205.
154. Quentin M, Allasia V, Pegard A, et al. 2009. Imbalanced lignin biosynthesis promotes the sexual reproduction of homothallic oomycete pathogens. PLoSPathogens 5: e1000264.
155. Ralph J, Brunow G, Harris PJ, Dixon RA, Schatz PF, Boerjan W. 2008. Lignification: are lignins biosynthesized via simple combinatorial chemistry or via proteinaceous control and template replication? Recent Advances in Polyphenol Research 1:36-66.
156. Ranocha P, McDougall G, Hawkins S, et al. 1999. Biochemical characterization, molecular cloning and expression of laccases-a divergent gene family-in poplar. European Journal of Biochemistry 259:485-495.
157. Ranocha P, Chabannes M, Chamayou S, et al. 2002. Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiology 129: 145-155.
158. Rastogi S, Kumar R, Chanotiya CS, et al. 2013.4-Coumarate:CoA ligase partitions metabolites for eugenol biosynthesis. Plant and Cell Physiology 54: 1238-1252.
159. Richardson A, McDougall GJ. 1997. A laccase-type polyphenol oxidase from lignifying xylem of tobacco. Phytochemistry 44: 229-235.
160. Ro DK, Mah N, Ellis BE, Douglas CJ. 2001. Functional characterization and subcellular localization of poplar (Populus trichocarpa x Populus del-toides) cinnamate 4-hydroxylase. Plant Physiology 126: 317-329.
161. Rogers LA, Dubos C, Cullis IF, et al. 2005. Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. Journal of Experimental Botany 56: 1651-1663.
162. Roppolo D, De Rybel B, Tendon VD, et al. 2011. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473: 380-383.
163. 2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207: 207-216.
164. 2 necessary for lignification in differentiating xylem vessels. Planta 220: 747-756.
165. Rozema J, van de Staaij J, Bjorn LO, Caldwell M. 1997. UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology and Evolution 12: 22-28.
166. Ruelland E, Campalans A, Selman-Housein G, Puigdomenech P, Rigau J. 2003. Cellular and subcellular localization of the lignin biosynthetic enzymes caffeic acid O-methyltransferase, cinnamyl alcohol dehydrogenase and cinnamoyl-Coenzyme A reductase in two monocots, sugarcane and maize. Physiologia Plantarum 117: 93-99.
167. Sagi M, Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141:336-340.
168. Samaj J, Hawkins S, Lauvergeat V, Grima-Pettenati J, Boudet A. 1998. Immunolocalization of cinnamyl alcohol dehydrogenase 2 (CAD 2) indicates a good correlation with cell-specific activity of CAD 2 promoter in transgenic poplar shoots. Planta 204:437-443.
169. Santiago LJM, Louro RP, De Oliveira DE. 2000. Compartmentation of phenolic compounds and phenylalanine ammonia-lyase in leaves of Phyllanthus tenellus Roxb. and their induction by copper sulphate. Annals of Botany 86: 1023-1032.
170. Sato K, Nishikubo N, Mashino Y, et al. 2009. Immunohistochemical localization of enzymes that catalyze the long sequential pathways of lignin biosynthesis during differentiation of secondary xylem tissues of hybrid aspen (Populus sieboldii x Populus grandidentata). Tree Physiology 29: 1599-1606.
171. Sato T, Takabe K, Fujita M. 2004. Immunolocalization of phenylalanine ammonia-lyase and cinnamate-4-hydroxylase in differentiating xylem of poplar. Comptes Rendus Biologies 327: 827-836.
172. Sato Y, Demura T, Yamawaki K, et al. 2006. Isolation and characterization of a novel peroxidase gene ZPO-C whose expression and function are closely associated with lignification during tracheary element differentiation. Plant and Cell Physiology 47:493-503.
173. Schopker H, Kneisel M, Beerhues L, Robenek H, Wiermann R. 1995. Phenylalanine ammonia-lyase and chalcone synthase in glands of Primula kewensis (W. Wats): immunofluorescence and immunogold localization. Planta 196: 712-719.
174. Schuetz M, Benske A, Smith RA, et al. 2014. Laccases direct lignification in the discrete secondary cell wall domains of protoxylem. Plant Physiology 166: 798-807.
175. Serk H, Gorzsas A, Tuominen H, Pesquet E. 2015. Cooperative lignification of xylem tracheary elements. Plant Signaling and Behavior (in press).
176. Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL. 2010. Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant and Cell Physiology 51: 144-163.
177. Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y. 2013. Putative cat-ionic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. Journal of Agricultural and Food Chemistry 61: 3781-3788.
178. Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y. 2015. Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. Journal of Integrative Plant Biology (in press).
179. Sibout R, Eudes A, Pollet B, et al. 2003. Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis. Isolation and characterization of the corresponding mutants. Plant Physiology 132: 848-860.
180. Smart CC, Amrhein N. 1985. The influence of lignification on the development of vascular tissue in Vigna radiata L. Protoplasma 124: 87-95.
181. Smith CG, Rodgers MW, Zimmerlin A, Ferdinando D, Bolwell GP. 1994. Tissue and subcellular immunolocalisation of enzymes of lignin synthesis in differentiating and wounded hypocotyl tissue of French bean (Phaseolus vulgaris L.). Planta 192: 155-164.
182. 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. The Plant Cell 25: 3988-3999.
183. Srivastava V, Schinkel H, Witzell J, et al. 2007. Downregulation of ligh-isoelecric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen. The Plant Journal 49: 135-148.
184. Stange RR, Ralph J, Peng JP, Sims JJ, Midland SL, McDonald RE. 2001. Acidolysis and hot water extraction provide new insights into the composition of the induced 'lignin-like' material from squash fruit. Phytochemistry 57: 1005-1011.
185. Sterjiades R, Dean JFD, Eriksson KEL. 1992. Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiology 99: 1162-1168.
186. Sterjiades R, Dean JFD, Gamble G, Himmelsbach DS, Eriksson KEL. 1993. Extracellular laccases and peroxidases from sycamore maple (Acer pseudoplatanus) cell-suspension cultures. Planta 190: 75-87.
187. Steudle E. 2000. Water uptake by roots: effects of water deficit. Journal of Experimental Botany 51: 1531-1542.
188. Sundin L, Vanholme R, Geerinck J, et al. 2014. Mutation of the inducible ARABIDOPSIS THALIANA CYTOCHROME P450 REDUCTASE2 alters lignin composition and improves saccharification. Plant Physiology 166: 1956-71.
189. Tahara K, Norisada M, Hogetsu T, Kojima K. 2005. Aluminum tolerance and aluminum-induced deposition of callose and lignin in the root tips of Melaleuca and Eucalyptus species. Journal of Forest Research 10: 325-333.
190. Takabe K, Fujita M, Harada H, Saiki H. 1985. Autoradiographic investigation of lignification in the cell walls of cryptomeria (Cryptomeria japonica D. Don). Mokuzai Gakkaishi 31: 613-619.
191. Takabe K, Takeuchi M, Sato T, Ito M, Fujita M. 2001. Immunocytochemical localization of enzymes involved in lignification of the cell wall. Journal of Plant Research 114: 509-515.
192. Takeuchi M, Takabe K, Fujita M. 2001. Immunolocalization of O-methyl-transferase and peroxidase in differentiating xylem of poplar. Holzforschung 55: 146-150.
193. 2 in a dialysis tube. I. Preparation of highly polymerized DHPs. Wood Research: Bulletin of the Wood Research Institute Kyoto University 67: 29-42.
194. Tao S, Khanizadeh S, Zhang H, Zhang S. 2009. Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species. Plant Science 176: 413-419.
195. Taylor JG, Owen TP, Koonce LT, Haigler CH. 1992. Dispersed lignin in tracheary elements treated with cellulose synthesis inhibitors provides evidence that molecules of the secondary cell wall mediate wall patterning. The Plant Journal 2: 959-970.
196. Temp U, Eggert C. 1999. Novel interaction between laccase and cellobiose de-hydrogenase during pigment synthesis in the white rot fungus Pycnoporus cinnabarinus. Applied Environmental Microbiology 65: 389-395.
197. Terashima N, Fukushima K. 1988. Heterogeneity in formation of lignin. XI. An autographic study of heterogeneous formation and structure of pine lig-nin. Wood Science and Technology 22: 259-270.
198. Terashima N, Fukushima K. 1989. Biogenesis and structure of macromolecular lignin in the cell wall of tree xylem as studied by microautoradiography. Plant Cell Wall Polymers: 160-168.
199. Terashima N, Yoshida M, Hafrén J, Fukushima K, Westermark U. 2012. Proposed supramolecular structure of lignin in softwood tracheid compound middle lamella regions. Holzforschung 66: 907-915.
200. Thévenin J, Pollet B, Letarnec B, et al. 2011. The simultaneous repression of CCR and CAD, two enzymes in the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Molecular Plant 4: 70-82.
201. Tobimatsu Y, Chen F, Nakashima J, et al. 2013. Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin polymers in seed coats. The Plant Cell 25: 2587-2600.
202. Tokunaga N, Sakakibara N, Umezawa T, Ito Y, Fukuda H, Sato Y. 2005. Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant and Cell Physiology 46: 224-232.
203. Tokunaga N, Kaneta T, Sato S, Sato Y. 2009. Analysis of expression profiles of three peroxidase genes associated with lignification in Arabidopsis thali-ana. Physiologia Plantarum 136: 237-49.
204. Torres MA, Jones JD, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiology 141: 373-378.
205. Tsuji Y, Fukushima K. 2004. Behavior of monolignol glucosides in angio-sperms. Journal of Agricultural and Food Chemistry 52: 7651-7659.
206. Tsutsumi Y, Matsui K, Sakai K. 1998. Substrate specific peroxidases in woody angiosperms and gymnosperms participate in regulating the dehydrogena-tive polymerisation of syringyl and guaiacyl type lignins. Holzforschung 52: 275-281.
207. Tsuyama T, Kawai R, Shitan N, et al. 2013. Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiology 162: 918-926
208. Turlapati, PV, Kim KW, Davin LB, Lewis NG. 2011. The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233: 439-470.
209. Turner SR, Somerville CR. 1997. Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. The Plant Cell 9: 689-701.
210. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Berlin: Springer.
211. Valério L, De Meyer M, Penel C, Dunand C. 2004. Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 65: 1331-1342.
212. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. 2010. Lignin biosynthesis and structure. Plant Physiology 153: 895-905.
213. Vanholme R, Cesarino I, Rataj K, et al. 2013. Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341: 1103-1106.
214. Vogt T. 2010. Phenylpropanoid biosynthesis. Molecular Plant 3: 2-20.
215. Wang JP, Shuford CM, Li Q, et al. 2012. Functional redundancy of the two 5-hydroxylases in monolignol biosynthesis of Populus trichocarpa. LC-MS/MS based protein quantification and metabolic flux analysis. Planta 236: 795-808.
216. Watts HD, Mohamed MNA, Kubicki JD. 2011. Comparison of multistandard and TMS-standard calculated NMR shifts for coniferyl alcohol and application of the multistandard method to lignin dimers. Journal of Physical Chemistry B 115: 1958-1970
217. Weng JK, Chapple C. 2010. The origin and evolution of lignin biosynthesis. New Phytologist 187: 273-285.
218. Whetten R, Sederoff R. 1995. Lignin biosynthesis. The Plant Cell 7: 1001-1013.
219. White PJ, Broadley MR. 2001. Chloride in soils and its uptake and movement within the plant: a review. Annals of Botany 88: 967-988.
220. Wilkerson CG, Mansfield SD, Lu F, et al. 2014. Monolignol ferulate transfer-ase introduces chemically labile linkages into the lignin backbone. Science 344: 90-93.
221. Wuyts N, Lognay R, Verscheure M, Marlier M, Waele DD, Swennen R. 2007. Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). Plant Pathology 56: 878-890.
222. Yang F, Mitra P, Zhang L, et al. 2013. Engineering secondary cell wall deposition in plants. Plant Biotechnology Journal 11: 325-335.
223. Ye ZH. 1997. Association of caffeoyl coenzyme A 3-O-methyltransferase expression with lignifying tissues in several dicot plants. Plant Physiology 115: 1341-1350.
224. Yoshimura K, Masuda A, Kuwano M, Yokota A, Akashi K. 2008. Programmed proteome response for drought avoidance/tolerance in the root of a C3 xerophyte (wild watermelon) under water deficits. Plant and Cell Physiology 49: 226-241.
225. Zeier J, Schreiber L. 1997. Chemical composition of hypodermal and endodermal cell walls and xylem vessels isolated from Clivia miniata (Identification of the biopolymers lignin and suberin). Plant Physiology 113: 1223-1231.
226. Zeier J, Ruel K, Ryser U, Schreiber L. 1999. Chemical analysis and immunolocalisation of lignin and suberin in endodermal and hypodermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots. Planta 209: 1-12.
227. Zhao Q, Nakashima J, Chen F, et al. 2013. LACCASE is necessary and non-redundant with PEROXIDASE for lignin polymerization during vascular development in arabidopsis. The Plant Cell 25: 3976-3987.
228. Zhong R, Morrison WH, Himmelsbach DS, Poole FL, Ye ZH. 2000. Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiology 124: 563-578.
229. Zhu Q, Dabi T, Beeche A, Yamamoto R, Lawton MA, Lamb C. 1995. Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase. Plant Molecular Biology 29: 535-550.
230. Zhu Y, Du B, Qian J, Zou B, Hua J. 2013. Disease resistance gene-induced growth inhibition is enhanced by rcd1 independent of defense activation in Arabidopsis. Plant Physiology 161: 2005-2013.