Abstract
Polymorphisms within three candidate genes for lignin biosynthesis were investigated to identify alleles useful for the improvement of maize digestibility. The allelic diversity of two caffeoyl-CoA 3-O-methyltransferase genes, CCoAOMT2 and CCoAOMT1, as well as that of the aldehyde O-methyltransferase gene, AldOMT, was evaluated for 34 maize lines chosen for their varying degrees of cell wall digestibility. Frequency of nucleotide changes averaged one SNP every 35 bp. Ninety-one indels were identified in non-coding regions and only four in coding regions. Numerous distinct and highly diverse haplotypes were identified at each locus. Numerous sites were in linkage disequilibrium that declined rapidly within a few hundred bases. For F4, an early flint French line with high cell wall digestibility, the CCoAOMT2 first exon presented many non-synonymous polymorphisms. Notably we found an 18-bp indel, which resembled a microsatellite and was associated with cell wall digestibility variation. Additionally, the CCoAOMT2 gene co-localized with a QTL for cell wall digestibility and lignin content. Together, these results suggest that genetic diversity investigated on a broader genetic basis could contribute to the identification of favourable alleles to be used in the molecular breeding of elite maize germplasm.
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References
Aufrére J, Michalet-Doreau B (1983) In vivo digestibility and prediction of digestibility of some by-products. IECC seminar, Belgique
Barrière Y, Gibelin C, Argillier O, Méchin V (2001) Genetic analysis and QTL mapping in forage maize based on recombinant inbred lines descended from the cross between F288 and F271. I. Yield, earliness starch and crude protein content. Maydica 46:253–266
Barrière Y, Guillet C, Goffner D, Pichon M (2003) Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Anim Res 52:193–228
Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register JC III, Tingey SV, Rafalski A (2002) Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546
Buckler ES IV, Thornsberry J (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111
Capellades M, Torres MA, Bastisch I, Stiefel V, Vignols F, Bruce WB, Peterson D, Puigdomenech P, Rigau J (1996) The maize caffeic acid O-methyltransferase gene promoter is active in transgenic tobacco and maize plant tissues. Plant Mol Biol 31:307–322
Collazo P, Montoliu L, Puigdomenech P, Rigau J (1992) Structure and expression of the lignin O-methyltransferase gene from Zea mays L. Plant Mol Biol 20:857–867
Cummings MP, Clegg MT (1998) Nucleotide sequence diversity at the alcohol dehydrogenase 1 locus in wild barley (Hordeum vulgare ssp. spontaneum): an evaluation of the background selection hypothesis. Proc Natl Acad Sci USA 95:5637–5642
Feldbrugge M, Sprenger M, Hahlbrock K, Weisshaar B (1997) PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J 11:1079–1093
Feuillet C, Lauvergeat V, Deswarte C, Pilate G, Boudet A, Grima-Pettenati J (1995) Tissue- and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol 27:651–667
Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Grimmig B, Matern U (1997) Structure of the parsley caffeoyl-CoA O-methyltransferase gene, harbouring a novel elicitor responsive cis-acting element. Plant Mol Biol 33:323–341
Guillet C, Barrière Y (2001) Polymorphismes du gène CCoAOMT2 de maïs, et leurs utilisations pour améliorer la digestibilité des plantes. Patent WO 03/054229
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
Guo D, Chen F, Wheeler J, Winder J, Selman S, Peterson M, Dixon RA (2001) Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res 10:457–464
Hanson MA, Gaut BS, Stec AO, Fuerstenberg SI, Goodman MM, Coe EH, Doebley JF (1996) Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. Genetics 143:1395–1407
Hilton H, Gaut BS (1998) Speciation and domestication in maize and its wild relatives: evidence from the globulin-1 gene. Genetics 150:863–872
Hoffmann L, Maury S, Bergdoll M, Thion L, Erard M, Legrand M (2001) Identification of the enzymatic active site of tobacco caffeoyl-coenzyme A O-methyltransferase by site-directed mutagenesis. J Biol Chem 276:36831–36838
Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164
Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Ibrahim RK, Bruneau A, Bantignies B (1998) Plant O-methyltransferases: molecular analysis, common signature and classification. Plant Mol Biol 36:1–10
Ito H, Hiraga S, Tsugawa H, Matsui H, Honma M, Otsuki Y, Murakami T, Ohashi Y (2000) Xylem-specific expression of wound-inducible rice peroxidase genes in transgenic plants. Plant Sci 155:85–100
Lorkovic ZJ, Wieczorek Kirk DA, Lambermon MH, Filipowicz W (2000) Pre-mRNA splicing in higher plants. Trends Plant Sci 5:160–167
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
Mogg R, Batley J, Hanley S, Edwards D, O’Sullivan H, Edwards J (2002) Characterization of the flanking regions of Zea mays microsatellites reveals a large number of useful sequence polymorphisms. Theor Appl Genet 105:532–543
Neustaedter DA, Lee SP, Douglas CJ (1999) A novel parsley 4CL1 cis-element is required for developmentally regulated expression and protein–DNA complex formation. Plant J 18:77–88
Osterberg MK, Shavorskaya O, Lascoux M, Lagercrantz U (2002) Naturally occurring indel variation in the Brassica nigra COL1 gene is associated with variation in flowering time. Genetics 161:299–306
Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806
Piquemal J, Chamayou S, Nadaud I, Beckert M, Barriere Y, Mila I, Lapierre C, Rigau J, Puigdomenech P, Jauneau A, Digonnet C, Boudet AM, Goffner D, Pichon M (2002) Down-regulation of caffeic acid o-methyltransferase in maize revisited using a transgenic approach. Plant Physiol 130:1675–1685
Poke FS, Vaillancourt RE, C ER, Reid BR (2003) Sequence variation in two lignin biosynthesis genes, cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD2). Mol Breed 12:107–118
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Rafalski A, Morgante M (2004) Corn and humans: recombination and linkage disequilibrium in two genomes of similar size. Trends Genet 20:103–111
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES IV (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Roussel V, Gibelin C, Fontaine AS, Barrière Y (2002) Genetic analysis in recombinant inbred lines of early dent forage. II. QTL mapping for cell wall constituents and cell wall digestibility from per se value and top cross experiments. Maydica 47:9–20
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
SAS Institute (1999) PROC REG software. SAS Institute, Cary
Small RL, Wendel JF (2002) Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol Biol Evol 19:597–607
Sokal RR, Rohlf FJ (1981) Biometry. Freeman, San Francisco
Solano R, Nieto C, Avila J, Canas L, Diaz I, Paz-Ares J (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 14:1773–1784
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166
Tenaillon MI, Sawkins MC, Anderson LK, Stack SM, Doebley J, Gaut BS (2002) Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.). Genetics 162:1401–1413
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES IV (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
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
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Whitbred JM, Schuler MA (2000) Molecular characterization of CYP73A9 and CYP82A1 P450 genes involved in plant defense in pea. Plant Physiol 124:47–58
Wilson WA, Harrington SE, Woodman WL, Lee M, Sorrells ME, McCouch SR (1999) Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated panicoids. Genetics 153:453–473
Zhang L, Peek AS, Dunams D, Gaut BS (2002) Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics 162:851–860
Acknowledgements
This work was supported by grants from the Genoplante maize program, coordinated by Alain Charcosset (INRA Le Moulon) and Alain Murigneux (Biogemma, Les Cézeaux). We thank Sabine Guillaumie, V. Méchin and M. Pichon for comments on the manuscript. We thank Jeremy l’Homedet for skilful technical assistance. We are very grateful to P-Ph. Claude for encouragement and help during manuscript preparation.
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Guillet-Claude, C., Birolleau-Touchard, C., Manicacci, D. et al. Genetic diversity associated with variation in silage corn digestibility for three O-methyltransferase genes involved in lignin biosynthesis. Theor Appl Genet 110, 126–135 (2004). https://doi.org/10.1007/s00122-004-1808-4
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DOI: https://doi.org/10.1007/s00122-004-1808-4