Skip to main content
Log in

Meta-analysis of QTL involved in silage quality of maize and comparison with the position of candidate genes

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

A meta-analysis of quantitative trait loci (QTL) associated with plant digestibility and cell wall composition in maize was carried out using results from 11 different mapping experiments. Statistical methods implemented in “MetaQTL” software were used to build a consensus map, project QTL positions and perform meta-analysis. Fifty-nine QTL for traits associated with digestibility and 150 QTL for traits associated with cell wall composition were included in the analysis. We identified 26 and 42 metaQTL for digestibility and cell wall composition traits, respectively. Fifteen metaQTL with confidence interval (CI) smaller than 10 cM were identified. As expected from trait correlations, 42% of metaQTL for digestibility displayed overlapping CIs with metaQTL for cell wall composition traits. Coincidences were particularly strong on chromosomes 1 and 3. In a second step, 356 genes selected from the MAIZEWALL database as candidates for the cell wall biosynthesis pathway were positioned on our consensus map. Colocalizations between candidate genes and metaQTL positions appeared globally significant based on χ2 tests. This study contributed in identifying key chromosomal regions involved in silage quality and potentially associated genes for most of these regions. These genes deserve further investigation, in particular through association mapping.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Andersen JR, Zein I, Wenzel G, Krützfeldt 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

    Article  CAS  PubMed  Google Scholar 

  • Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20:2324–2326

    Article  CAS  PubMed  Google Scholar 

  • Argillier O, Barrière Y (1996) Valeur alimentaire et inscription des variétés de maïs ensilage aux catalogues officiels en Europe. Fourrages 146:131–140

    Google Scholar 

  • Argillier O, Méchin V, Barrière Y (2000) Inbred line evaluation and breeding for digestibility-related traits in forage maize. Crop Sci 40:1596–1600

    Google Scholar 

  • Argillier O, Barrière Y, Lila M, Jeanneteau K, Gélinet K, Menanteau V (1996) Genotypic variation in phenolic components of cell-wall in relation to the digestibility of maize stalks. Agronomie 16:123–130

    Article  Google Scholar 

  • 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 46:256–266

    Google Scholar 

  • Barrière Y, Guillet-Claude 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

  • 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

    Article  PubMed  Google Scholar 

  • Barrière Y, Riboulet C, Méchin V, Maltese S, Pichon M, Cardinal A, Lapierre C, Martinant JP (2007) Genetics and genomics of lignification in grass cell walls based on maize as model species. Genes Genomes Genomics 1:133–156

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Barrière Y, Méchin V, Lafarguette F, Manicacci D, Guillon F, Wang H, Lauressergues D, Pichon M, Bosio H, Tatout C (2009) Toward the discovery of maize cell wall genes involved in silage maize quality and capacity to biofuel production. Maydica 54

  • Beló A, Zheng P, Luck S, Shen B, Meyer DJ, Li B, Tingey S, Rafalski A (2007) Whole genome scan detects an allelic variant of fad2 associated with increased oleic acid levels in maize. Mol Gen Genomics 279:1–10

    Article  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546

    Article  CAS  PubMed  Google Scholar 

  • Bohn M, Schulz B, Kreps R, Klein D, Melchinger AE (2000) QTL mapping for resistance against the European corn borer (Ostrinia nubilalis H.) in early maturing European dent germplasm. Theor Appl Genet 101:907–917

    Article  CAS  Google Scholar 

  • Boitard S, Abdallah J, de Rochambeau H, Cierco-Ayrolles C, Mangin B (2006) Linkage disequilibrium interval mapping of quantitative trait loci. BMC Genomics 7:54

    Google Scholar 

  • Bortiri E, Jackson D, Hakel S (2006) Advances in maize genomics: the emergence of positional cloning. Curr Opin Plant Biol 9:164–171

    Article  CAS  PubMed  Google Scholar 

  • Cardinal AJ, Lee M, Moore KJ (2003) Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize. Theor Appl Genet 106:866–874

    Google Scholar 

  • Causse M, Santoni S, Damerval C, Maurice A, Charcosset A, Deatrick J, Vienne D (1996) A composite map of expressed sequences in maize. Genome 39:418–432

    Article  CAS  PubMed  Google Scholar 

  • Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A (2004) Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168:2169–2185

    Article  CAS  PubMed  Google Scholar 

  • Darvasi A, Soller M (1997) A simple method to calculate resolving power and confidence interval of QTL map location. Behav Genet 27:125–132

    Article  CAS  PubMed  Google Scholar 

  • Dence CW, Lin SY (1992) The determination of lignin. In: Dence CW, Lin SY (eds) Methods in lignin chemistry. Springer, Berlin, pp 33–61

  • Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52:17–27

    Article  CAS  PubMed  Google Scholar 

  • Emerson RA (1935) Memoir 180. Agricultural Experiment Station, Cornell University, Ithaca

    Google Scholar 

  • Fontaine AS, Briand M, Barriere Y (2003) Genetic variation and QTL mapping of para-coumaric and ferulic acid contents in maize stover at silage harvest. Maydica 48:75–84

    Google Scholar 

  • Goering HK, Van Soest PJ (1970) Forage fiber analysis (apparatus, reagents, procedures and some applications). Agricultural handbook 379 US Gov Print Office, Washington, DC, 57 pp

  • Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis, vol 155. Genetics Society of America, pp 463–473

  • Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326(5956):1115–1117

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J (2009) Meta-QTL analysis of the genetic control of ear emergence in elite European winter wheat germplasm. Theor Appl Genet 119:383–395

    Article  CAS  PubMed  Google Scholar 

  • Guillaumie S, Pichon M, Martinant JP, Bosio H, Goffner D, Barrière Y (2007a) Differential expression of phenylpropanoid and related genes in brown-midrib bm1, bm2, bm3, and bm4 young near-isogenic maize plants. Planta 226:235–250

    Article  CAS  PubMed  Google Scholar 

  • Guillaumie S, San-Clemente H, Deswarte C, Martinez Y, Lapierre C, Murigneux A, Barrière Y, Pichon M, Goffner D (2007b) MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize. Plant Physiol 173:339–363

    Google Scholar 

  • Guillaumie S, Goffner D, Barbier O, Martinant JP, Pichon M, Barrière 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

    Google Scholar 

  • Guillet-Claude C, Birolleau-Touchard C, Manicacci D, Fourmann M, Barraud S, Carret V, Martinant JP, Barrière Y (2004) Genetic diversity associated with variation in silage corn digestibility for three O-methyltransferase genes involved in lignin biosynthesis. Theor Appl Genet 110:126–135

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hanocq E, Laperche A, Jaminon O, Lainé A-L, Le Gouis J (2007) Most significant regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Park CM (2007) Vascular development in plants: specification of xylem and phloem tissues. J Plant Biol 50:301–305

    Article  CAS  Google Scholar 

  • Khowaja FS, Norton GJ, Courtois B, Price AH (2009) Improved resolution in the position of drought-related QTLs in a single mapping population of rice by meta-analysis. BMC Genomics 10:276

    Article  PubMed  Google Scholar 

  • Krakowsky MD, Lee M, Beeghly HH, Coors JG (2003) Characterization of quantitative trait loci affecting fiber and lignin in maize (Zea Mays L.). Maydica 48:283–292

    Google Scholar 

  • Krakowsky MD, Lee M, Coors JG (2005) Quantitative trait loci for cell-wall components in recombinant inbred lines of maize (Zea mays L.) I: stalk tissue. Theor Appl Genet 111:337–346

    Article  CAS  PubMed  Google Scholar 

  • Krakowsky MD, Lee M, Coors JG (2006) Quantitative trait loci for cell wall components in recombinant inbred lines of maize (Zea mays L.) II: leaf sheath tissue. Theor Appl Genet 112:717–726

    Article  CAS  PubMed  Google Scholar 

  • Lacombe E, Hawkins S, Doorsselaere JV, Piquemal J, Goffner D (1997) Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. Plant J 11:429–441

    Article  CAS  PubMed  Google Scholar 

  • Löffler M, Schön CC, Miedaner T (2009) Revealing the genetic architecture of FHB resistance in hexaploid wheat (Triticum aestivum L.) by QTL meta-analysis. Mol Breed 23:473–488

    Article  Google Scholar 

  • Lübberstedt T, Melchinger AE, Schön CC, Utz HF, Klein D (1997a) QTL mapping in testcrosses of European flint lines of maize: I. Comparison of different testers for forage yield traits. Crop Sci 37:921–931

    Article  Google Scholar 

  • Lübberstedt T, Melchinger AE, Klein D, Degenhardt H, Paul C (1997b) QTL mapping in testcrosses of European flint lines of maize: II. Comparison of different testers for forage quality traits. Crop Sci 37:1913–1922

    Article  Google Scholar 

  • Madson M, Dunand C, Li X, Vermab R, Vanzin GF, Caplanb J, Shouea DA, Nicholas CC, Reiter W-D (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670

    Article  CAS  PubMed  Google Scholar 

  • Marandel G, Salava J, Abbott A, Candresse T, Decroocq V (2009) Quantitative trait loci meta-analysis of Plum pox virus resistance in apricot (Prunu armeniaca L.): new insights on the organization and the identification of genomic resistance factors. Mol Plant Pathol 10(3):347–360

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Méchin V, Argillier O, Hebert 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

    Article  Google Scholar 

  • Michailidis G, Argirou A, Darzentas N, Tsaftaris A (2009) Analysis of xyloglucan endotransglycosylase/hydrolase (XTH) genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors expressed during fiber elongation. J Plant Physiol 166:403–416

    Article  CAS  PubMed  Google Scholar 

  • Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Höfte H (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013

    Article  CAS  PubMed  Google Scholar 

  • Papst C, Melchinger AE, Eder J, Schulz B, Klein D, Bohn M (2001) 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 46:195–205

    Google Scholar 

  • Penning BW, Hunter CT 3rd, Tayengwa R, Eveland AL, Dugard CK, Olek AT, Vermerris W, Koch KE, McCarty DR, Davis MF, Thomas SR, McCann MC, Carpita NC (2009) Genetic resources for maize cell wall biology. Plant Physiol 151:1703–1728

    Article  CAS  PubMed  Google Scholar 

  • Provan GJ, Scobbie L, Chesson A (1997) Characterisation of lignin from CAD- and OMT-deficient bm mutants of maize. J Sci Food Agric 73:133–142

    Article  CAS  Google Scholar 

  • Riboulet C, Fabre F, Denoue D, Martinant JP, Lefevre B, Barriere Y (2008) QTL mapping and candidate gene research from lignin content and cell wall digestibility in a top-cross of a flint maize recombinant inbred line progeny harvested at silage stage. Maydica 53:1–9

    Google Scholar 

  • Rong J, Feltus FA, Waghmare VJ, Pierce GJ, Chee PW, Draye X, Saranga Y, Wright RJ, Wilkins TA, May OL, Smith CW, Gannaway JR, Wendel JF, Paterson AH (2007) Meta-analysis of polyploid cotton QTL shows unequal contributions of subgenomes to a complex network of genes and gene clusters implicated in Lint fiber development. Genetics 176:2577–2588

    Article  CAS  PubMed  Google Scholar 

  • Roussel V, Gibelin C, Fontaine AS, Barriere 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 pre se value and top cross experiments. Maydica 47:9–20

    Google Scholar 

  • Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski JA, Tingey SV, Miao GH, Phillips RL, Tuberosa R (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104:11376–11381

    Article  CAS  PubMed  Google Scholar 

  • Šamaj 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(4):437–443

    Google Scholar 

  • Schaeffer ML, Sanchez-Villeda H, McMullen MD, Coe E (2006) IBM2 2005 Neighbors—45,000 Locus resource for maize. Plant and animal genome conference, p 200

  • Sen TZ, Andorf CM, Schaeffer ML, Harper LC, Sparks ME, Duvick J, Brendel VP, Cannon E, Campbell DA, Lawrence CJ (2009) MaizeGDB becomes ‘sequence-centric’ database, 2009 bap020

  • Shi C, Koch G, Ouzunova M, Wenzel G, Zein I, Lubberstedt T (2006) Comparison of maize brown-midrib isogenic lines by cellular UV-microspectrophotometry and comparative transcript profiling. Plant Mol Biol 62:697–714

    Article  CAS  PubMed  Google Scholar 

  • Shi C, Uzarowska A, Ouzunova M, Lanbeck M, Wenzel G, Lübberstedt T (2007) Identification of candidate genes associated with cell wall digestibility and eQTL (expression quantitative trait loci) analysis in a Flint × Flint maize recombinant inbred lines population. BMC Genomics 8:22

    Google Scholar 

  • Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182:851–861

    Article  CAS  PubMed  Google Scholar 

  • Tateishi A, Mori H, Watari J, Nagashima K, Yamaki S, Inoue H (2005) Isolation, characterization, and cloning of {alpha}-l-Arabinofuranosidase expressed during fruit ripening of Japanese pear. Plant Physiol 138:1653–1664

    Article  CAS  PubMed  Google Scholar 

  • Thomas BR, Inouhe M, Simmons CR, Nevins DJ (2000) Endo-1,3;1,4-beta-glucanase from coleoptiles of rice and maize: role in the regulation of plant growth. Int J Biol Macromol 27:145–149

    Article  CAS  PubMed  Google Scholar 

  • Thomas J, Guillaumie S, Verdu D, Pichon M, Barriere Y (2010) Cell wall phenylpropanoid-related gene expression in early maize recombinant inbred lines differing in parental alleles at a major lignin QTL position. Mol Breed 25:105

    Article  CAS  Google Scholar 

  • Veyrieras JB, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinformatics 8:49

    Article  PubMed  Google Scholar 

  • Vielle-Calzada JP, Martínez de la Vega O, Hernández-Guzmán G, Ibarra-Laclette E, Alvarez-Mejía C, Vega-Arreguín JC, Jiménez-Moraila B, Fernández-Cortés A, Corona-Armenta G, Herrera-Estrella L, Herrera-Estrella A (2009) The Palomero genome suggests metal effects on domestication. Science 326:1071–1072

    Article  Google Scholar 

  • Wei F, Zhang J, Zhou S, He R, Schaeffer M, Collura K, Kudrna D, Faga BP, Wissotski M, Golser W, Rock SM, Graves TA, Fulton RS, Coe E, Schnable PS, Schwartz DC, Ware D, Clifton SW, Wilson RK, Wing RA (2009) The physical and genetic framework of the maize B73 genome. PLoS Genet 5(11):e1000715

    Google Scholar 

  • Wongvithoonyaporn P, Bucke C, Svasti J (1998) Separation, characterization, and specificity of alpha-mannosidases from Vigna umbellata. Biosci Biotechnol Biochem 62:613–621

    Article  CAS  PubMed  Google Scholar 

  • Yu JM, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–551

    Article  PubMed  Google Scholar 

  • Zhong R, Kaysb SJ, Schroederb BP, Ye Z-H (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Jean-Baptiste Veyrieras for his help regarding the use of MetaQTL software, Cedric Muller and Florence Servant for Blast of candidate genes from “Maizewall” to the maizesequence database, Olivier Sosnowski for help in informatics computations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Truntzler.

Additional information

Communicated by T. Luebberstedt.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Truntzler, M., Barrière, Y., Sawkins, M.C. et al. Meta-analysis of QTL involved in silage quality of maize and comparison with the position of candidate genes. Theor Appl Genet 121, 1465–1482 (2010). https://doi.org/10.1007/s00122-010-1402-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-010-1402-x

Keywords

Navigation