[en] Fifteen quantitative trait loci (QTL) for cell wall digestibility and lignin content were shown in the recombinant inbred line (RIL) progeny descended from the cross between F288 and F271, two early dent lines of contrasted cell wall digestibility. Among these QTL, those located in bin 6.06, respectively explained 20 and 40% of the phenotypic variation for lignin content and cell wall digestibility. Expression of genes related to cell wall and lignin biosynthesis was investigated with the ‘‘MaizeWall’’ macro-array in two RIL having favorable alleles for low lignin content and high cell wall digestibility, except in bin 6.06 where RIL39 and RIL99 had unfavorable and favorable alleles, respectively. In the lignin pathway, three PAL, 4CL1, ZmCCR1, COMT, and ZmCAD2 genes were under-expressed in RIL99 in comparison to RIL39. In addition, two cytochrome P450, ZmCHS, and ZmCHI1 genes were simultaneously under-expressed while F5H2 and two OMT ZRP4-like genes were over-expressed. However, none of these genes were mapped in bin 6.06. Based on maize–rice synteny and on Maize Genome Sequencing Project data, several putative candidate genes related to lignin content and lignified tissue patterning were found in the support interval of bin 6.06 QTL. These genes included one C30H which is likely the missing constitutive gene of the maize lignin pathway. Three ZRP4-like OMT were also
shown in the support interval of the QTL. However, their involvement in the lignin pathway has not yet been firmly established. Several regulation or transcription factors were also shown in the QTL support interval. Among them, MYB, zinc finger, bZIP, and COV1 genes belong to families with members involved in lignification regulation or in lignified tissue patterning. In addition, auxin response factors have been shown to be indirectly involved in plant lignification. Moreover, several genes encoding proteins of unknown function and genes annotated ‘‘retrotransposon-like’’ were also located in the QTL support interval. Current results are not conclusive on the candidate gene discovery, but strengthen the hypothesis that regulation genes are better candidates than genes involved in the monolignol pathway. Fine mapping, association genetics, and/or functional validation have to be considered for more definite conclusions.
Disciplines :
Genetics & genetic processes
Author, co-author :
Thomas, Justine; UGAPF, INRA de Lusignan - Université Paul Sabatier
Guillaumie, Sabine; UGAPF, INRA de Lusignan - Université Paul Sabatier
Verdu, Cindy ; UGAPF, INRA de Lusignan - Université de Poitiers
Denoue, Dominique; UGAPF, INRA de Lusignan
Pichon, Magalie; UGAPF, INRA de Lusignan - Université Paul Sabatier
Barrière, Yves; UGAPF, INRA de Lusignan
Language :
English
Title :
Cell wall phenylpropanoid-related gene expression in early maize recombinant inbred lines differing in parental alleles at a major lignin QTL position
Publication date :
2010
Journal title :
Molecular Breeding
ISSN :
1380-3743
eISSN :
1572-9788
Publisher :
Springer Science & Business Media B.V., Dordrecht, Netherlands
Abdulrazzak N, Pollet B, Ehlting J, Larsen K, Asnaghi C, Ronseau S, Proux C, Erhardt M, Seltzer V, Renou JP, Ullmann P, Pauly M, Lapierre C, Werck-Reichhart D (2006) A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growth. Plant Physiol 140: 30-48.
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
Andersen JR, Zein I, Wenzel G, Krutzfeldt B, Eder J, Ouzunova M, Lübberstedt T (2007) High levels of linkage disequilibrium and associations with forage quality at a phenylalanine ammonia-lyase locus in European maize (Zea mays L.) inbreds. Theor Appl Genet 114: 307-319.
Argillier O, Barrière Y, Hébert Y (1995) Genetic variation and selection criterion for digestibility traits of forage maize. Euphytica 82: 175-184.
Argillier O, Méchin V, Barrière Y (2000) Inbred line evaluation and breeding for digestibility-related traits in forage maize. Crop Sci 40: 1596-1600.
Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242.
Aufrère J, Michalet-Doreau B (1983) In vivo digestibility and prediction of digestibility of some by-products. EEC seminar, 26-29 September 1983, Mlle Gontrode, Belgium, pp 25-33.
Barrière Y, Gibelin C, Argillier O, Méchin V (2001) Genetic analysis in recombinant inbred lines of early dent forage maize. I-QTL mapping for yield, earliness, starch and crude protein contents from per se value and top cross experiments. Maydica 46: 253-266.
Barrière Y, Surault F, Emile JC (2003) Genetic variation of silage maize ingestibility in dairy cattle. Anim Res 52: 489-500.
Barrière Y, Ralph J, Méchin V, Guillaumie S, Grabber JH, Argillier O, Chabbert B, Lapierre C (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C R Biol 327: 847-860.
Barrière Y, Riboulet C, Méchin V, Maltese S, Pichon M, Cardinal AJ, Lapierre C, Lübberstedt T, Martinant JP (2007) Genetics and genomics of lignification in grass cell walls based on maize as a model system. Genes, Genomes and Genomics 1: 133-156.
Barrière Y, Thomas J, Denoue D (2008) QTL mapping for lignin content, lignin monomeric composition, p-hydroxycinnamate content, and cell wall digestibility in the maize recombinant inbred line progeny F838 × F286. Plant Sci 175: 585-595.
Barrière Y, Méchin V, Lafarguette F, Manicacci D, Guillon F, Wang H, Lauressergues D, Pichon M, Bosio M, Tatout C (2009) Towards the discovery of maize cell wall genes involved in silage quality and capability to biofuel production. Maydica (submitted).
Boddu J, Jiang C, Sangar V, Olson T, Peterson T, Chopra S (2006) Comparative structural and functional characterization of sorghum and maize duplications containing orthologous Myb transcription regulators of 3-deoxyflavonoid biosynthesis. Plant Mol Biol 60: 185-199.
Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JE, Blais S, Tremblay L, Morency MJ, Pavy N, Grima-Pettenati J, Séguin A, Mackay J (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59: 3925-3939.
Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126: 524-535.
Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Mérillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140: 499-511.
Dence CW, Lin SY (1992) The determination of lignin. In: Lin SY, Dence CW (eds) Methods in lignin chemistry. Springer-Verlag, Berlin, pp 33-61.
Dolstra O, Medema JH (1990) An effective screening method for genetic improvement of cell-wall digestibility in forage maize. Proceedings of the 15th Eucarpia maize and sorghum congress, Baden, Austria, J Hinterholzer, Federal Institute for Plant Production, A-1201, Vienne Ed, pp 258-270.
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366-371.
Eulgem T, Rushton P, Robatzek S, Somssich I (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206.
Falque M, Decousset L, Dervins D, Jacob AM, Joets J, Martinant JP, Raffoux X, Ribiere N, Ridel C, Samson D, Charcosset A, Murigneux A (2005) Linkage mapping of 1454 new maize candidate gene loci. Genetics 170: 1957-1966.
Fontaine AS, Briand M, Barrière Y (2003) Genetic variation and QTL mapping of para-coumaric and ferulic acid contents in maize stover at silage harvest. Maydica 48: 75-82.
Fornale S, Sonbol FM, Maes T, Capellades M, Puigdomenech P, Rigau J, Caparros-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.
Franken P, Schrell S, Peterson PA, Saedler H, Wienand U (1994) Molecular analysis of protein domain function encoded by the Myb-homologous maize gene-C1, gene-Zm-1 and gene-Zm-38. Plant J 6: 21-30.
Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277: 696-699.
Glawischnig E, Grun S, Frey M, Gierl A (1999) Cytochrome P450 monooxygenases of DIBOA biosynthesis: specificity and conservation among grasses. Phytochemistry 50: 925-930.
Goering HK, van Soest PJ (1970) Forage fiber analysis (apparatus, reagents, procedures and some applications), US Government Printing Office, Washington.
Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati G (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43: 553-567.
Grabber JH (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45: 820-831.
Grabber JH, Ralph J, Hatfield RD (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agric Food Chem 46: 2609-2614.
Grabber JH, Ralph J, Lapierre C, Barrière Y (2004) Genetic and molecular basis of grass cell-wall degradability. I. Lignin-cell wall matrix interactions. C R Biol 327: 455-465.
Grotewold E, Peterson T (1994) Isolation and characterization of a maize gene encoding chalcone flavonone isomerase. Mol Gen Genet 242: 1-8.
Guillaumie S, San-Clemente H, Deswarte C, Martinez Y, Lapierre C, Murigneux A, Barrière Y, Pichon M, Goffner D (2007a) MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize. Plant Physiol 143: 339-363.
Guillaumie S, Pichon M, Martinant JP, Bosio M, Goffner D, Barrière Y (2007b) Differential expression of phenylpropanoid and related genes in brown-midrib bm1, bm2, bm3, and bm4 young near-isogenic maize plants. Planta 226: 235-250.
Guillaumie S, Goffner D, Barbier O, Martinant JP, Pichon M, Barriere Y (2008) Expression of cell wall related genes in basal and ear internodes of silking brown-midrib-3, caffeic acid O-methyltransferase (COMT) down-regulated, and normal maize plants. BMC Plant Biol 8: 71.
Guillet-Claude C, Birolleau-Touchard C, Manicacci D, Rogowsky PM, Rigau J, Murigneux A, Martinant JP, Barrière Y (2004) Nucleotide diversity of the ZmPox3 maize peroxidase gene: relationships between a MITE insertion in exon 2 and variation in forage maize digestibility. BMC Genet 5: 19.
Halpin C, Holt K, Chojecki J, Oliver D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon GA (1998) Brown-midrib maize (bm1)-a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant J 14: 545-553.
Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131: 1089-1100.
Hatfield RD, Jung HJG, Ralph J, Buxton DR, Weimer PJ (1994) A comparison of the insoluble residues produced by the klason lignin and acid detergent lignin procedures. J Sci Food Agric 65: 51-58.
Hatfield RD, Ralph J, Grabber JH (1999) Cell wall cross-linking by ferulates and diferulates in grasses. J Sci Food Agric 79: 403-407.
Held BM, Wang HQ, John I, Wurtele ES, Colbert JT (1993) An messenger-RNA putatively coding for an O-methyltransferase accumulates preferentially in maize roots and is located predominantly in the region of the endodermis. Plant Physiol 102: 1001-1008.
Higuchi T, Ito Y, Kawamura I (1967) p-Hydroxyphenyl component of grass lignin and the role of tyrosine ammonia-lyase in its formation. Phytochemistry 6: 875-881.
Jacquet G, Pollet B, Lapierre C (1995) New ether-linked ferulic acid-coniferyl alcohol dimers identified in grass straws. J Agric Food Chem 43: 2746-2751.
Jakoby M, Weisshaar B, Dröge-Laser W, Vincente-Carbojosa J, Tindemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7: 106-111.
Jung HG, Mertens DR, Payne AJ (1997) Correlation of acid detergent lignin and Klason lignin with digestibility of forage dry matter and neutral detergent fiber. J Dairy Sci 80: 1622-1628.
Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol 56: 255-270.
Klun JA, Tipton CL, Rindle TA (1967) 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA), an active agent in the resistance of maize to the European corn borer. J Econ Entomol 60: 1529-1533.
Krakowsky M, Lee M, Beeghly H, Coors J (2003) Characterization of quantitative trait loci affecting fiber and lignin in maize (Zea mays L.). Maydica 48: 283-292.
Lübberstedt T, Melchinger A, Klein D, Degenhardt H, Paul C (1997) QTL mapping in testcrosses of European flint lines of maize: II. Comparison of different testers for forage quality traits. Crop Sci 37: 1913-1922.
Lübberstedt T, Melchinger A, Fahr S, Klein D, Dally A, Westhoff P (1998) QTL mapping in testcrosses of flint lines of maize: III. Comparison across populations for forage traits. Crop Sci 38: 1278-1289.
Méchin V, Argillier O, Menanteau V, Barrière Y, Mila I, Pollet B, Lapierre C (2000) Relationship of cell wall composition to in vitro cell wall digestibility of maize inbred line stems. J Sci Food Agric 80: 574-580.
Méchin V, Argillier O, Hébert Y, Guingo E, Moreau L, Charcosset A, Barrière Y (2001) Genetic analysis and QTL mapping of cell wall digestibility and lignification in silage maize. Crop Sci 41: 690-697.
Méchin V, Argillier O, Rocher F, Hébert Y, Mila I, Pollet B, Barrière Y, Lapierre C (2005) In search of a maize ideotype for cell wall enzymatic degradability using histological and biochemical lignin characterization. J Agric Food Chem 53: 5872-5881.
Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138: 1083-1096.
Melchinger AE, Utz HF, Schön CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149: 383-403.
Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19: 270-280.
Morant M, Schoch GA, Ullmann P, Ertunc T, Little D, Olsen CE, Petersen M, Negrel J, Werck-Reichhart D (2007) Catalytic activity, duplication and evolution of the CYP98 cytochrome P450 family in wheat. Plant Mol Biol 63: 1-19.
Morrison WH, Akin DE, Himmelsbach DS, Gamble GR (1993) Investigation of the ester-linked and ether-linked phenolic constituents of cell-wall types of normal and brown-midrib pearl-millet using chemical isolation, microspectrophotometry and C-13 NMR-spectroscopy. J Sci Food Agric 63: 329-337.
Morrison TA, Jung HG, Buxton DR, Hatfield RD (1998) Cell wall composition of maize internodes of varying maturity. Crop Sci 38: 455-460.
Moyano E, MartinezGarcia JF, Martin C (1996) Apparent redundancy in Myb gene function provides gearing for the control of flavonoid biosynthesis in Antirrhinum flowers. Plant Cell 8: 1519-1532.
Naoumkina MA, He XZ, Dixon RA (2008) Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula. BMC Plant Biol 8: 132.
Paponov IA, Teale WD, Trebar M, Blilou K, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10: 170-177.
Parker G, Schofield R, Sundberg B, Turner S (2003) Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development 130: 2139-2148.
Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36: 743-754.
Paz-Ares J, Ghosal D, Wienand U, Peterson P, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to MYB proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6: 3553-3558.
Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SI, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16: 1898-1911.
Pesquet E, Ranocha P, Legay S, Digonnet C, Barbier O, Pichon M, Goffner D (2005) Novel markers of xylogenesis in Zinnia are differentially regulated by auxin and cytokinin. Plant Physiol 139: 1-19.
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 9: e45.
Price AH (2006) Believe it or not, QTLs are accurate!. Trends Plant Sci 11: 213-216.
Ralph J, Kim H, Lu F, Grabber JH, Leple JC, Berrio-Sierra J, Derikvand MM, Jouanin L, Boerjan W, Lapierre C (2008) Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency). Plant J 53: 368-379.
Rengel D, San-Clemente H, Servant F, Ladouce N, Paux E, Wincker P, Couloux A, Sivadon P, Grima-Pettenati J (2009) A new genomic resource dedicated to wood formation in Eucalyptus. BMC Plant Biol 9: 36.
Riboulet C, Fabre F, Dénoue D, Martinant JP, Lefèvre B, Barrière Y (2008a) QTL mapping and candidate gene research for lignin content and cell wall digestibility in a top-cross of a flint maize recombinant inbred line progeny harvest at silage stage. Maydica 83: 1-9.
Riboulet C, Lefèvre B, Denoue D, Barrière Y (2008b) Genetic variation in maize cell wall for lignin content, lignin structure, p-hydroxycinnamic acid content, and digestibility in a set of 19 lines at silage harvest maturity. Maydica 53: 11-19.
Riboulet C, Guillaumie S, Méchin V, Bosio M, Pichon M, Goffner D, Lapierre C, Pollet B, Lefèvre B, Martinant JP, Barrière Y (2009) Kinetics of phenylpropanoid gene expression in maize growing internodes: relationships with cell wall deposition. Crop Sci 49: 211-223.
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Gandehari D, Sherman BK, Yu CL (2000) Arabidopsis transcription factors, genome wide comparative analysis among eukaryotes. Science 290: 2105-2110.
Roadhouse FE, MacDougall D (1956) A study of the nature of plant lignin by means of alkaline nitrobenzene oxidation. Biochem J 63: 33-39.
Roesler J, Krekel F, Amrhein N, Schmid J (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol 113: 175-179.
Rose A, Meier I, Wienand U (1999) The tomato I-box binding factor LeMYBI is a member of a novel class of myb-like proteins. Plant J 20: 641-652.
Roussel V, Gibelin C, Fontaine AS, Barrière Y (2002) 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: 9-20.
Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25: 836-847.
Sanchez JP, Ullman C, Moore M, Choo Y, Chua NH (2006) Regulation of Arabidopsis thaliana 4-coumarate: coenzyme-A ligase-1 expression by artificial zinc finger chimeras. Plant Biotechnol J 4: 103-114.
Schöch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3 '-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Bio Chem 276: 36566-36574.
Sonbol FM, Fornalé S, Cappellades M, Encina A, Tourino S, Torres JL, Rovira P, Ruel K, Puigdomenech P, Rigau J, Caparros-Ruiz D (2009) The maize ZmMYB42 represses the phenylpropanoid pathway and affects the cell wall structure, composition and degradability in Arabidopsis thaliana. Plant Mol Biol 70: 283-296.
Struik P (1983) Physiology of forage maize (Zea mays L.) in relation to its production and quality. Ph. Dissertation, Agricultural University, 6700 GW Wageningen, The Netherlands, pp 1-252.
Utz H, Melchinger A (1996) PLABQTL: a program for composite interval mapping of QTL. J Agric Genomics 2: 1-6.
Utz HF, Melchinger AE, Schön CC (2000) Bias and sampling errors of the estimates proportion of genotypic variance explained by quantitative traits loci determined from experimental data in maize using cross validation and validation with independent samples. Genetics 154: 1839-1849.
Vignols F, Rigau J, Torres MA, Capellades M, Puigdomenech P (1995) The brown midrib3 (Bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7: 407-416.
Wayne ML, McIntyre LM (2002) Combining mapping and arraying: an approach to candidate gene identification. Proc Natl Acad Sci U S A 99: 14903-14906.
Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, Fuks G, Sanchez-Villeda H, Schroeder S, Fang Z, McMullen M, Davis G, Bowers JE, Paterson AH, Schaeffer M, Gardiner J, Cone K, Messing J, Soderlund C, Wing RA (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3: 1254-1263.
Wissenbach M, Uberlacker B, Vogt F, Becker D, Salamini F, Rohde W (1993) MYB genes from Hordeum vulgare-tissue-specific expression of chimeric MYB Promoter/Gus genes in transgenic tobacco. Plant J 4: 411-422.
Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55: 652-664.
Yin Y, Zhu Q, Dai S, Lamb C, N'Beachy R (1997) RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development. EMBO J 16: 5247-5259.
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.
Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19: 2776-2792.
Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20: 2763-2782.
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.
