Genetic and molecular basis of grass cell-wall biosynthesis and degradability. III. Towards a forage grass ideotype

Comptes Rendus - Biologies

Volumn 327, Issue 5, 2004, Pages 467-479

  Ralph, John ^a   Guillaumie, Sabine ^b   Grabber, John H ^a   Lapierre, Catherine ^c   Barrière, Yves ^b  

^a U S DAIRY FORAGE RESEARCH CENTER   (United States)

^b CEMAGREF   (France)

^c AGROPARISTECH   (France)

Author keywords

Cell wall; Digestibility; Genetic resources; Grass; Lignin

Indexed keywords

CAFFEIC ACID DERIVATIVE; CATECHOL METHYLTRANSFERASE; CELL MEMBRANE PROTEIN; LIGNIN; PARA COUMARIC ACID;

DIGESTIBILITY; LIGNIN;

ALLELE; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL WALL; CONTROLLED STUDY; ENZYME DEGRADATION; FORAGE; GENE CLUSTER; GENE IDENTIFICATION; GENE LOCATION; GENETIC ENGINEERING; GENETIC VARIABILITY; GERMPLASM; GRASS; LIGNIFICATION; MAIZE; MOLECULAR GENETICS; NONHUMAN; PLANT BREEDING; PLANT CELL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; QUANTITATIVE TRAIT LOCUS;

ANIMAL FEED; ANIMALS; CELL WALL; DIGESTION; GENETIC ENGINEERING; LIGNIN; POACEAE;

POACEAE; ZEA MAYS;

EID: 2942590825     PISSN: 16310691     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.crvi.2004.03.004     Document Type: Article

References (102)

1. Barrière Y. Guillet C. Goffner D. Pichon M. Genetic variation and breeding strategies for improved cell-wall digestibility in annual forage crops. A review Anim. Res. 52 2003 193-228
2. Grabber J.H. Ralph J. Lapierre C. Barrière Y. Genetic and molecular basis of grass cell-wall biosynthesis and degradability. I. Components and structure of cell walls in grasses C. R. Biologies 2004
3. Barrière Y. Ralph J. Méchin V. Guillaumie S. Grabber J.H. Argillier O. Chabbert B. Lapierre C. Genetic and molecular basis of grass cell-wall biosynthesis and degradability. II. Lessons from brown-midrib mutants C. R. Biologies 2004
4. Lübberstedt T. Melchinger A.E. Klein D. Degenhardt H. Paul C. QTL mapping in testcrosses of European flint lines of maize. 2. Comparison of different testers for forage quality traits Crop Sci. 37 1997 1913-1922
5. Lübberstedt T. Melchinger A.E. Fahr S. Klein D. Dally A. Westhoff P. QTL mapping in testcrosses of flint lines of maize: III. Comparison across populations for forage traits Crop Sci. 38 1998 1278-1289
6. Méchin V. Argillier O. Hebert Y. Guingo E. Moreau L. Charcosset A. Barrière Y. Genetic analysis and QTL mapping of cell-wall digestibility and lignification in silage maize Crop Sci. 41 2001 690-697
7. Roussel V. Gibelin C. Fontaine A.S. Barrière Y. Genetic analysis in recombinant inbred lines of early dent forage maize. II. QTL mapping for cell-wall constituents and cell-wall digestibility from per se value and top cross experiments Maydica 47 2002 9-20
8. Cardinal A.J. Lee M. Moore K.J. Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize Theor. Appl. Genet. 106 2003 866-874
9. Maize Genetics and Genomics Database http://www.maizegdb.org
10. Flint-Garcia S.A. Jampatong C. Darrah L.L. McMullen M.D. Quantitative trait locus analysis of stalk strength in four maize populations Crop Sci. 43 2003 13-22
11. S. Marhadour, Introduction de la fétuque dans le ray-grass au niveau tétraploïde. Approche morphogénétique et apports du marquage moléculaire, PhD thesis, École nationale supérieure agronomique de Rennes, Rennes, France, 2001
12. Barrière Y. Argillier O. In vivo silage feeding value of early maize hybrids released in France between 1958 and 1994 Euphytica 99 1997 175-182
13. Lauer J.G. Coors J.G. Flannery P.J. Forage yield and quality of corn cultivars developed in different eras Crop Sci. 41 2001 1449-1455
14. O. Argillier, Relations entre verses, valeur alimentaire et productivité chez le maïs fourrage, PhD thesis, Institut national agronomique, Paris-Grignon, France, 1995
15. Travis A.J. Murison S.D. Hirst D.J. Walker K.C. Chesson A. Comparison of the anatomy and degradability of straw from varieties of wheat and barley that differ in susceptibility to lodging J. Agric. Sci. 127 1996 1-10
16. Boudet A.-M. Lignins and lignification: selected issues Plant Physiol. Biochem. 38 2000 81-96
17. Dixon R.A. Chen F. Guo D.J. Parvathi K. The biosynthesis of monolignols: a 'metabolic grid', or independent pathways to guaiacyl and syringyl units? Phytochemistry 57 2001 1069-1084
18. Humphreys J.M. Chapple C. Rewriting the lignin roadmap Curr. Opin. Plant Biol. 2002 224-229
19. Boerjan W. Ralph J. Baucher M. Lignin Biosynthesis Annu. Rev. Plant Biol. 54 2003 519-549
20. Higuchi T. Pathways for monolignol biosynthesis via metabolic grids: coniferyl aldehyde 5-hydroxylase, a possible key enzyme in angiosperm syringyl lignin biosynthesis Proc. Jap. Acad. Ser. B: Phys. Biol. Sci. 79 2003 227-236
21. Boudet A.-M. Towards an understanding of the supramolecular organization of the lignified wall Rose J. The Plant Cell Wall Annu. Plant Rev. 8 2003 155-182
22. Chen C.Y. Baucher M. Christensen J.H. Boerjan W. Biotechnology in trees: towards improved paper pulping by lignin engineering Euphytica 118 2001 185-195
23. Piquemal J. Chamayou S. Nadaud I. Beckert M. Barrière Y. Mila I. Lapierre C. Rigau J. Puigdomenech P. Jauneau A. Digonnet C. Boudet A.-M. Goffner D. Pichon M. Down-regulation of caffeic acid O-methyltransferase in maize revisited using a transgenic approach Plant Physiol. 130 2002 1675-1685
24. He X. Hall M.B. Gallo-Meagher M. Smith R.L. Improvement of forage quality by downregulation of maize O-methyltransferase Crop Sci. 43 2003 2240-2251
25. Chen L. Auh C.-K. Dowling P. Bell J. Chen F. Hopkins A. Dixon R.A. Wang Z.-Y. Improved forage digestibility of tall fescue (Festuca arundinacea) by transgenic down-regulation of cinnamyl alcohol dehydrogenase Plant Biotechnol. J. 1 2003 437-449
26. Grabber J.H. Ralph J. Hatfield R.D. Quideau S. p-Hydroxyphenyl, Guaiacyl, and syringyl lignins have similar inhibitory effects on wall degradability J. Agric. Food Chem. 45 1997 2530-2532
27. Halpin C. Foxon G.A. Fentem P.A. Transgenic plants with improved energy characteristics Chesson A. Wallace R.J. Biotechnology in Animal Feeds and Animal Feeding 1995 279-293 VCH Weinheim, Germany
28. Casler M.D. Kaeppler H.F. Molecular breeding for herbage quality in forage crops Spangenberg G. Molecular Breeding of Forage Crops 2001 175-188 Kluwer Academic Dordecht, The Netherlands
29. Anterola A.M. Lewis N.G. Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity Phytochemistry 61 2002 221-294
30. Ehlting J. Buttner D. Wang Q. Douglas C.J. Somssich I.E. Kombrink E. Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms Plant J. 19 1999 9-20
31. Hu W.-J. Kawaoka A. Tsai C.-J. Lung J. Osakabe K. Ebinuma H. Chiang V.L. Compartmentalized expression of two structurally and functionally distinct 4-coumarate coenzyme A ligase genes in aspen (Populus tremuloides) Proc. Natl Acad. Sci. USA 95 1998 5407-5412
32. Baucher M. Bernard-Vailhe M.A. Chabbert B. Besle J.M. Opsomer C. Van Montagu M. Botterman J. Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility Plant Mol. Biol. 39 1999 437-447
33. Bernard-Vailhe M.-A. Cornu A. Robert D. Maillot M.-P. Besle J.-M. Cell-wall degradability of transgenic tobacco stems in relation to their chemical extraction and lignin quality J. Agric. Food Chem. 44 1996 1164-1169
34. Gordon A.J. Neudoerffer T.S. Chemical and in vivo evaluation of a brown midrib mutant of Zea mays. I. Fiber, lignin, and amino acid composition and digestibility for sheep J. Sci. Food Agric. 24 1973 565-577
35. Barrière Y. Argillier O. Chabbert B. Tollier M.-T. Monties B. Breeding silage maize with brown-midrib genes - Feeding value and biochemical characteristics Agronomie 14 1994 15-25
36. Grabber J.H. Ralph J. Hatfield R.D. Severe inhibition of maize wall degradation by synthetic lignins formed with coniferaldehyde J. Sci. Food Agric. 78 1998 81-87
37. Li L.G. Cheng X.F. Leshkevich J. Umezawa T. Harding S.A. Chiang V.L. The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase Plant Cell 13 2001 1567-1585
38. Sibout R. Eudes A. Pollet B. Goujon T. Mila I. Granier F. Seguin A. Lapierre C. Jouanin L. Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis, Isolation and characterization of the corresponding mutants Plant Physiol. 132 2003 848-860
39. Halpin C. Knight M.E. Foxon G.A. Campbell M.M. Boudet A.-M. Boon J.J. Chabbert B. Tollier M.-T. Schuch W. Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase Plant J. 6 1994 339-350
40. Boudet A.-M. Grima-Pettenati J. Lignin genetic engineering Mol. Breed. 2 1996 25-39
41. Lapierre C. Pollet B. Petit-Conil M. Toval G. Romero J. Pilate G. Leple J.C. Boerjan W. Ferret V. De Nadai V. Jouanin L. Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping Plant Physiol. 119 1999 153-163
42. Grima-Pettenati J. Goffner D. Lignin genetic engineering revisited Plant Sci. 145 1999 51-65
43. Baucher M. Christensen J.H. Meyermans H. Chen C.Y. Van Doorsselaere J. Leple J.C. Pilate G. Petit-Conil M. Jouanin L. Chabbert B. Monties B. Van Montagu M. Boerjan W. Applications of molecular genetics for biosynthesis of novel lignins Polym. Degrad. Stabil. 59 1998 47-52
44. Lapierre C. Pollet B. Petit-Conil M. Pilate G. Leple C. Boerjan W. Jouanin L. Genetic engineering of poplar lignins: impact of lignin alteration on kraft pulping performances Lignin: Historical, Biological, and Materials Perspectives 742 2000 145-160
45. Pilate G. Guiney E. Holt K. Petit-Conil M. Lapierre C. Leple J.C. Pollet B. Mila I. Webster E.A. Marstorp H.G. Hopkins D.W. Jouanin L. Boerjan W. Schuch W. Cornu D. Halpin C. Field and pulping performances of transgenic trees with altered lignification Nat. Biotechnol. 20 2002 607-612
46. Baucher M. Chabbert B. Pilate G. Van Doorsselaere J. Tollier M.-T. Petit-Conil M. Cornu D. Monties B. Van Montagu M. Inze D. Jouanin L. Boerjan W. Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar Plant Physiol. 112 1996 1479-1490
47. O'Connell A. Holt K. Piquemal J. Grima-Pettenati J. Boudet A. Pollet B. Lapierre C. Petit-Conil M. Schuch W. Halpin C. Improved paper pulp from plants with suppressed cinnamoyl-CoA reductase or cinnamyl alcohol dehydrogenase Transgenic Res. 11 2002 495-503
48. Dimmel D.R. MacKay J.J. Althen E. Parks C. Boon J.J. Pulping, bleaching, and characterization of CAD-deficient wood 10th Int. Symp. on Wood and Pulping Chemistry Yokohama, Japan, vol. 1 1999 524-527
49. Dimmel D.R. MacKay J.J. Althen E. Parks C. Boon J.J. Pulping and bleaching of CAD-deficient wood J. Wood Chem. Technol. 21 2001 1-18
50. Piquemal J. Lapierre C. Myton K. O'Connell A. Schuch W. Grima-Pettenati J. Boudet A.-M. Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants Plant J. 13 1998 71-83
51. Ralph J. Hatfield R.D. Piquemal J. Yahiaoui N. Pean M. Lapierre C. Boudet A.-M. NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamyl-alcohol dehydrogenase and cinnamoyl-CoA reductase Proc. Natl Acad. Sci. 95 1998 12803-12808
52. Chabannes M. Ruel K. Yoshinaga A. Chabbert B. Jauneau A. Josseleau J.-P. Boudet A.-M. In situ analysis of specifically engineered tobacco lignins reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and sub-cellular levels Plant J. 28 2001 271-282
53. Goujon T. Ferret V. Mila I. Pollet B. Ruel K. Burlat V. Joseleau J.-P. Barrière Y. Lapierre C. Jouanin L. Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability Planta 217 2003 218-228
54. Abbott J.C. Barakate A. Pincon G. Legrand M. Lapierre C. Mila I. Schuch W. Halpin C. Simultaneous suppression of multiple genes by single transgenes. Down-regulation of three unrelated lignin biosynthetic genes in tobacco Plant Physiol. 128 2002 844-853
55. Chabannes M. Barakate A. Lapierre C. Marita J. Ralph J. Pean M. Danoun S. Halpin C. Grima-Pettenatia J. Boudet A.-M. Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants Plant J. 28 2001 257-270
56. Pincon G. Chabannes M. Lapierre C. Pollet B. Ruel K. Joseleau J.-P. Boudet A.-M. Legrand M. Simultaneous down-regulation of caffeic/5-hydroxy ferulic acid-O-methyltransferase I and cinnamoyl-coenzyme a reductase in the progeny from a cross between tobacco lines homozygous for each transgene. Consequences for plant development and lignin synthesis Plant Physiol. 126 2001 145-155
57. Jouanin L. Goujon T. de Nadaï V. Martin M.-T. Mila I. Vallet C. Pollet B. Yoshinaga A. Chabbert B. Petit-Conil M. Lapierre C. Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity Plant Physiol. 123 2000 1363-1373
58. Ralph J. Lapierre C. Marita J. Kim H. Lu F. Hatfield R.D. Ralph S.A. Chapple C. Franke R. Hemm M.R. Van Doorsselaere J. Sederoff R.R. O'Malley D.M. Scott J.T. MacKay J.J. Yahiaoui N. Boudet A.-M. Pean M. Pilate G. Jouanin L. Boerjan W. Elucidation of new structures in lignins of CAD- and COMT-deficient plants by NMR Phytochemistry 57 2001 993-1003
59. Lapierre C. Kim H. Lu F. Marita J.M. Mila I. Pollet B. Ralph J. Marker compounds for enzyme deficiencies in the lignin biosynthetic pathway 11th Int. Symp. Wood and Pulping Chemistry ('Association technique de l'industrie papetière' (ATIP), Paris & Nice, France), vol. II 2001 23-26
60. Marita J.M. Ralph J. Hatfield R.D. Guo D. Chen F. Dixon R.A. Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase Phytochem. 62 2003 53-65
61. Ralph J. Marita J. Lu F. Hatfield R.D. Lapierre C. Ralph S.A. Vermerris W. Boerjan W. Jouanin L. 5-Hydroxyconiferyl alcohol as a monolignol in COMT-deficient angiosperms 11th Int. Symp. Wood and Pulping Chemistry ('Association technique de l'industrie papetière' (ATIP), Paris & Nice, France), vol. II 2001 27-30
62. Hu W.-J. Lung J. Harding S.A. Popko J.L. Ralph J. Stokke D.D. Tsai C.-J. Chiang V.L. Repression of lignin biosynthesis in transgenic trees promotes cellulose accumulation and growth Nat. Biotechnol. 17 1999 808-812
63. Nair R.B. Bastress K.L. Ruegger M.O. Denault J.W. Chapple C. The Arabidopsis thaliana REDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis Plant Cell 16 2004 544-554
64. Guo D.G. Chen F. Wheeler J. Winder J. Selman S. Peterson M. Dixon R.A. Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases Transgenic Res. 10 2001 457-464
65. Chen C.Y. Meyermans H. Burggraeve B. De Rycke R.M. Inoue K. De Vleesschauwer V. Steenackers M. Van Montagu M.C. Engler G.J. Boerjan W.A. Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar Plant Physiol. 123 2000 853-867
66. Franke R. Hemm M.R. Denault J.W. Ruegger M.O. Humphreys J.M. Chapple C. Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis Plant J. 30 2002 47-59
67. Schoch G. Goepfert S. Morant M. Hehn A. Meyer D. Ullmann P. Werck-Reichhart D. CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway J. Biol. Chem. 276 2001 36566-36574
68. Sewalt V.J.H. Ni W.T. Jung H.G. Dixon R.A. Lignin impact on fiber degradation: increased enzymatic digestibility of genetically engineered tobacco (Nicotiana tabacum) stems reduced in lignin content J. Agric. Food Chem. 45 1997 1977-1983
69. Méchin V. Argillier O. Menanteau V. Barrière Y. Mila I. Pollet B. Lapierre C. Relationship of cell wall composition to in vitro cell-wall digestibility of maize inbred line stems J. Sci. Food Agric. 80 2000 574-580
70. Jung H.-J.G. Ni W. Chapple C.C.S. Meyer K. Impact of lignin composition on cell-wall degradability in an Arabidopsis mutant J. Sci. Food Agric. 79 1999 922-928
71. Li L. Zhou Y. Cheng X. Sun J. Marita J.M. Ralph J. Chiang V.L. Combinatorial modification of multiple lignin traits in trees through multigene cotransformation Proc. Natl Acad. Sci. USA 100 2003 4939-4944
72. Huntley S.K. Ellis D. Gilbert M. Chapple C. Mansfield S.D. Significant increases in pulping efficiency in C4H-F5H-transformed poplars: improved chemical savings and reduced environmental toxins J. Agric. Food Chem. 51 2003 6178-6183
73. Marita J. Ralph J. Hatfield R.D. Chapple C. NMR characterization of lignins in Arabidopsis altered in the activity of ferulate-5-hydroxylase Proc. Natl Acad. Sci. USA 96 1999 12328-12332
74. Ralph J. An unusual lignin from Kenaf J. Nat. Prod. 59 1996 341-342
75. Barcelo A.R. Peroxidase and not laccase is the enzyme responsible for cell-wall lignification in the secondary thickening of xylem vessels in Lupinus Protoplasma 186 1995 41-44
76. Ranocha P. Chabannes M. Chamayou S. Danoun S. Jauneau A. Boudet A.-M. Goffner D. Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar Plant Physiol. 129 2002 145-155
77. Syrjanen K. Brunow G. Regioselectivity in lignin biosynthesis. The influence of dimerization and cross-coupling J. Chem. Soc. Perkin Trans. 1 2000 183-187
78. Gang D.R. Costa M.A. Fujita M. Dinkova-Kostova A.T. Wang H.B. Burlat V. Martin W. Sarkanen S. Davin L.B. Lewis N.G. Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis Chem. Biol. 6 1999 143-151
79. J. Ralph, K. Lundquist, G. Brunow, F. Lu, H. Kim, P.F. Schatz, J.M. Marita, R.D. Hatfield, W. Boerjan, Lignins and lignification: current issues, Phytochem. Rev. (submitted)
80. Lewis N.G. Davin L.B. Sarkanen S. The nature and function of lignins Barton D.H.R. Nakanishi K. Comprehensive Natural Products Chemistry vol. 3 1999 617-745 Elsevier
81. Lim E.K. Li Y. Parr A. Jackson R. Ashford D.A. Bowles D.J. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis J. Biol. Chem. 276 2001 4344-4349
82. Tamagnone L. Merida A. Parr A. Mackay S. Culianez-Macia F.A. Roberts K. Martin C. The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco Plant Cell 10 1998 135-154
83. Rabinowicz P.D. Braun E.L. Wolfe A.D. Bowen B. Grotewold I. Maize R2R3 Myb genes: sequence analysis reveals amplification in the higher plants Genetics 153 1999 427-444
84. Kawaoka A. Ebinuma H. Transcriptional control of lignin biosynthesis by tobacco LIM protein Phytochemistry 57 2001 1149-1157
85. Sakurai N. Katayama Y. Yamaya T. Overlapping expression of cytosolic glutamine synthetase and phenylalanine ammonia-lyase in immature leaf blades of rice Physiol. Plant. 113 2001 400-408
86. Ito H. Hiraga S. Tsugawa H. Matsui H. Honma M. Otsuki Y. Murakami T. Ohashi Y. Xylem-specific expression of wound-inducible rice peroxidase genes in transgenic plants Plant Sci. 155 2000 85-100
87. Wilson W.A. Harrington S.E. Woodman W.L. Lee M. Sorrells M.E. McCouch S.R. Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated panicoids Genetics 153 1999 453-473
88. Haigler C.H. From signal-transduction to biophysics - tracheary element differentiation as a model system Int. J. Plant Sci. 155 1994 248-250
89. Ye Z.H. Vascular tissue differentiation and pattern formation in plants Annu. Rev. Plant Biol. 53 2002 183-202
90. The Arabidopsis Genome Initiative http://www.nsf.gov/od/lpa/news/media/ 2000/fsarabidopsis.htm
91. Costa M.A. Collins R.E. Anterola A.M. Cochrane F.C. Davin L.B. Lewis N.G. An in silico assessment of gene function and organization of the phenylpropanoid pathway metabolic networks in Arabidopsis thaliana and limitations thereof Phytochemistry 64 2003 1097-1112
92. Allona I. Quinn M. Shoop E. Swope K. St Cyr S. Carlis J. Riedl J. Retzel E. Campbell M.M. Sederoff R. Whetten R.W. Analysis of xylem formation in pine by cDNA sequencing Proc. Natl Acad. Sci. USA 95 1998 9693-9698
93. Sterky F. Regan S. Karlsson J. Hertzberg M. Rohde A. Holmberg A. Amini B. Bhalerao R. Larsson M. Villarroel R. Van Montagu M. Sandberg G. Olsson O. Teeri T.T. Boerjan W. Gustafsson P. Uhlen M. Sundberg B. Lundeberg J. Gene discovery in the wood-forming tissues of poplar: analysis of 5692 expressed sequence tags Proc. Natl Acad. Sci. USA 95 1998 13330-13335
94. Milioni D. Sado P.E. Stacey N.J. Domingo C. Roberts K. McCann M.C. Differential expression of cell-wall-related genes during the formation of tracheary elements in the Zinnia mesophyll cell system Plant Mol. Biol. 47 2001 221-238
95. Holtorf H. Guitton M.C. Reski R. Plant functional genomics Naturwissenschaften 89 2002 235-249
96. Fontaine A.S. Briand M. Barrière Y. Genetic variation and QTL mapping of para-coumaric and ferulic acid contents in maize stover at silage harvest Maydica 48 2003 75-82
97. Schön C.C. Lee M. Melchinger A.E. Guthrie W.D. Woodman W.L. Mapping and characterization of quantitative trait loci affecting resistance against 2nd-generation European corn-borer in maize with the aid of Rflps Heredity 70 1993 648-659
98. Bohn M. Schulz B. Kreps R. Klein D. Melchinger A.E. QTL mapping for resistance against the European corn borer (Ostrinia nubilalis H.) in early maturing European dent germplasm Theor. Appl. Genet. 101 2000 907-917
99. Cardinal A.J. Lee M. Sharopova N. Woodman-Clikeman W.L. Long M.J. Genetic mapping and analysis of quantitative trait loci for resistance to stalk tunneling by the European corn borer in maize Crop Sci. 41 2001 835-845
100. Papst C. Melchinger A.E. Eder J. Schulz B. Klein D. Bohn M. QTL mapping for resistance to European corn borer (Ostrinia nubilalis HB.) in early maturing European dent maize (Zea mays L.) germplasm and comparison of genomic regions for resistance across two populations of F3 families Maydica 46 2001 195-205
101. Jampatong C. McMullen M.D. Barry B.D. Darrah L.L. Byrne P.F. Kross H. Quantitative trait loci for first- and second-generation European corn borer resistance derived from the maize inbred Mo47 Crop Sci. 42 2002 584-593
102. Krakowsky M.D. Lee M. Woodman-Clikeman W.L. Long M.J. Sharopova N. QTL mapping of resistance to stalk tunneling by the European corn borer in RILs of maize population B73 × De811 Crop Sci. 44 2004 274-282