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Association mapping for wood quality and growth traits in Eucalyptus globulus ssp. globulus Labill identifies nine stable marker-trait associations for seven traits

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Abstract

The moderate to high levels of nucleotide diversity and low linkage disequilibrium found in many forest tree species make them ideal candidates for association mapping. Here, we report candidate gene-based association mapping results for complex wood quality and growth traits in Eucalyptus globulus Labill. ssp. globulus, the most widely grown eucalypt in temperate regions of the world. Ninety-eight single nucleotide polymorphisms (SNPs) from 20 wood quality candidate genes were assayed in a discovery population consisting of 385 trees sourced from a provenance-progeny trial. Twenty-five selected SNPs with significant associations (P < 0.05) in the discovery population were assayed for validation in 296 trees sourced from an independent second-generation breeding trial. To account for background genetic structure, mixed models were used in the association analyses. Two associations identified in the discovery population were independently supported in the validation testing. However, combining the discovery and validation results in a combined analysis, we discovered nine stable marker-trait associations for seven traits. These associations link underlying complex wood and growth phenotypes to earlier putative selection signatures opening new avenues to accelerate the dissection of these traits.

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References

  • Abramson JH (2004) WINPEPI (PEPI-for-Windows): computer programs for epidemiologists Epidemiologic Perspectives & Innovations 1:6

  • Astle W, Balding DJ (2009) Population structure and cryptic relatedness in genetic association studies. Stat Sci 24:451–471

    Article  Google Scholar 

  • Balding DJ (2006) A tutorial on statistical methods for population association studies. Nat Rev Genet 7:781–791

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu J et al (2011) Association genetics of wood physical traits in the conifer white spruce and relationships with. Gene Expr Genet 188:197–214

    CAS  Google Scholar 

  • Boerjan W, Polle A, Vander Mijnsbrugge K (2006) A role in lignification and growth for plant phenylcoumaran benzylic ether reductase US patent 2006/0015967

  • Bottcher Y et al (2009) Adipose tissue expression and genetic variants of the bone morphogenetic protein receptor 1A gene (BMPR1A) are associated with human obesity. Diabetes (New York) 58:2119–2128

    Google Scholar 

  • Bouakaze C et al (2011) Matrix-assisted laser desorption Ionization-time of flight mass spectrometry-based single nucleotide polymorphism genotyping assay using iPLEX gold technology for identification of mycobacterium tuberculosis complex species and lineages. J Clin Microbiol 49:3292–3299. doi:10.1128/jcm.00744-11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ram-doss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. doi:10.1093/bioinformatics/btm308

    Article  PubMed  CAS  Google Scholar 

  • Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proceedings of the National Academy of Sciences of the United States of America 101:15255–15260

  • Cappa EP, El-Kassaby YA, Garcia MN, Acuña C, Borralho NMG, Grattapaglia D, Marcucci Poltri SN (2013) Impacts of population structure and analytical models in genome-wide association studies of complex traits in forest trees: a case study in Eucalyptus globulus. PLoS ONE 8:e81267. doi:10.1371/journal.pone.0081267

  • Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure Proceedings of the National Academy of Sciences 106:13118–13123

  • Davidovich O, Kimmel G, Shamir R (2007) GEVALT: an integrated software tool for genotype analysis BMC. Bioinformatics 8:36

    PubMed  PubMed Central  Google Scholar 

  • Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Phys 50:245–276. doi:10.1146/annurev.arplant.50.1.245

    Article  CAS  Google Scholar 

  • Dillon SK, Nolan M, Li W, Bell C, Wu HX, Southerton SG (2010) Allelic variation in cell wall candidate genes affecting solid wood properties in natural populations and land races of Pinus radiata. Genetics 185:1477–1487

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Dutkowski GW, Potts BM (1999) Geographic patterns of genetic variation in eucalyptus globulus ssp. Globulus and a revised racial classification. Aust J Bot 47:237–263

    Article  Google Scholar 

  • Eckert AJ et al (2009) Association genetics of coastal Douglas fir (pseudotsuga menziesii var. Menziesii, pinaceae). I. Cold-Hardiness Related Traits. Genetics 182:1289–1302

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  PubMed  CAS  Google Scholar 

  • Eveno E et al (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437

    Article  PubMed  CAS  Google Scholar 

  • Fagard M et al (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of arabidopsis. Plant Cell 12:2409–2423

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Freeman J, Potts B, Downes G, Thavamanikumar S, Pilbeam D, Hudson C, Vaillancourt R (2011) QTL analysis for growth and wood properties across multiple pedigrees and sites in Eucalyptus globulus. BMC Proceedings 5:O8

  • Freeman JS, Potts BM, Downes GM, Pilbeam D, Thavamanikumar S, Vaillancourt RE (2013) Stability of quantitative trait loci for growth and wood properties across multiple pedigrees and environments in Eucalyptus globulus. New Phytol 198:1121–1134. doi:10.1111/nph.12237

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195–1206

    Article  PubMed  CAS  Google Scholar 

  • Garrick DJ, Taylor JF and Fernando RL (2009) Degressing estimated breeding values and weighting information for genomic regression analyses. Genet Sel Evol 41:55

  • Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plant Cell 15:1502–1506

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gonzalez-Martınez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006) DNA sequence variation and selection of tag single-nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1915–1926

    Article  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Martınez SC, Huber D, Ersoz E, Davis JM, Neale DB (2008) Association genetics in Pinus taeda L. II. Carbon isotope discrimination Heredity 101:19–26

  • Gonzalez-Martınez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I wood property traits. Genetics 175:399–409

    Article  PubMed  PubMed Central  Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2) Available from http://www2.unilch/popgen/softwares/fstat.htm

  • Grattapaglia D, Kirst M (2008) Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytol 179:911–929

    Article  PubMed  CAS  Google Scholar 

  • Hadjigol S (2012) Evidence for natural selection acting on genes affecting lignin and cellulose biosynthesis in Eucalyptus globulus (MSc thesis). University of Tasmania

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hernandez-Blanco C et al (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. IPlant Cell 19:890–903. doi:10.1105/tpc.106.048058

    Article  CAS  Google Scholar 

  • Hirschhorn JN, Altshuler D (2002) Once and again—issues surrounding replication in genetic association studies journal of clinical endocrinology. Metabolism 87:4438–4441

    CAS  Google Scholar 

  • Holliday JA, Ritland K, Aitken SN (2010) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytol 188:501–514

    Article  PubMed  Google Scholar 

  • Hu WJ et al (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17:808–812

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilbrium within and among natural populations of European aspen (Populus tremula L., salicaceae). Genetics 169:945–953

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178:2217–2226

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ivashuta S et al (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921. doi:10.1105/tpc.105.035394

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jallow M et al (2009) Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet 41:657–665. doi:10.1038/ng.388

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jones TH, Steane DA, Jones RC, Pilbeam D, Vaillancourt RE, Potts BM (2006) Effects of domestication on genetic diversity in Eucalyptus globulus. For Ecol Manage 234:78–84

    Article  Google Scholar 

  • Kalluri UC, Joshi CP (2004) Differential expression patterns of two cellulose synthase genes are associated with primary and secondary cell wall development in aspen trees. Planta 220:47–55. doi:10.1007/s00425-004-1329-z

    Article  PubMed  CAS  Google Scholar 

  • Kathiresan S et al (2008) Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat Genet 40:189–197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kawaoka A, Nanto K, Ishii K, Ebinuma H (2006) Reduction of lignin content by suppression of expression of the LIM domain transcription factor in Eucalyptus camaldulensis. Silvae Genet 55:269–277

    Google Scholar 

  • Kemper KE, Daetwyler HD, Visscher PM, Goddard ME (2012) Comparing linkage and association analyses in sheep points to a better way of doing GWAS. Genet Res 94:191–203. doi:10.1017/S0016672312000365

    Article  CAS  Google Scholar 

  • Kiselev KV, Turlenko AV, Zhuravlev YN (2010) Structure and expression profiling of a novel calcium-dependent protein kinase gene PgCDPK1a in roots, leaves, and cell cultures of Panax ginseng plant cell tissue and organ. Culture 103:197–204

    CAS  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kulheim C, Yeoh SH, Wallis IR, Laffan S, Moran GF, Foley WJ (2011) The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus. New Phytol 191:1041–1053

    Article  PubMed  CAS  Google Scholar 

  • Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1082. doi:10.1038/nprot.2009.86

    Article  PubMed  CAS  Google Scholar 

  • Kwon M, Davin LB, Lewis NG (2001) In situ hybridization and immunolocalization of lignan reductases in woody tissues: implications for heartwood formation and other forms of vascular tissue preservation. Phytochemistry 57:899–914. doi:10.1016/s0031-9422(01)00108-x

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Schork NJ (1994) Genetic dissection of complex traits. Science 265:2037–2048

    Article  PubMed  CAS  Google Scholar 

  • Lepoittevin C, Harvengt L, Plomion C, Garnier-Géré P (2012) Association mapping for growth, straightness and wood chemistry traits in the Pinus pinaster Aquitaine breeding population. Tree Genet Genom 8:113–126

    Article  Google Scholar 

  • Li A, Wang X, Leseberg CH, Jia J, Mao L (2008) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L). Plant Signal Behav 3:654–656

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma X-F, Hall D, Onge SKR, Janson S, Ingvarsson PK (2010) Genetic differentiation clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 186:1033–1044

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McRae TA, Pilbeam DJ, Powell MD, Joyce GW, Tier KB Genetic evaluation in eucalypt breeding programs. In: Borralho NMG, Pereira JS, Marques C, Coutinho J, Madeira M, Tomé M (eds) Eucalyptus in a changing world, Aveiro, Portugal, 11-15 October 2004. RAIZ, Instituto Investigação de Floresta e Papel, pp 189–190

  • Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829

    PubMed  CAS  PubMed Central  Google Scholar 

  • Munafo MR, Flint J (2004) Meta-analysis of genetic association studies trends. Genetics 20:439–444. doi:10.1016/j.tig.2004.06.014

    CAS  Google Scholar 

  • Ng PC, Henikoff S (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31:3812–3814. doi:10.1093/nar/gkg509

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1,4–D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. The EMBO Journal 17:5563–5576

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Patzlaff A et al (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754

    Article  PubMed  CAS  Google Scholar 

  • Pot D, McMillan L, Echt C, Le Provost G, Garnier-Gere P, Cato S, Plomion C (2005) Nucleotide variation in genes involved in wood formation in two pine species. New Phytol 167:101–112

    Article  PubMed  CAS  Google Scholar 

  • Pot D et al (2006) QTLs and candidate genes for wood properties in maritime pine (Pinus pinaster Ait). Tree Genet Genom 2:10–24

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genet 67:170–181

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qiu D, Wilson IW, Gan S, Washusen R, Moran GF, Southerton SG (2008) Gene expression in eucalyptus branch wood with marked variation in cellulose microfibril orientation and lacking G-layers. New Phytol 179:94–103

    Article  PubMed  CAS  Google Scholar 

  • Quesada T et al (2010) Association mapping of quantitative disease resistance in a natural population of loblolly pine (Pinus taeda L). Genetics 186:677–686

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ranik M, Myburg AA (2006) Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. Tree Physiol 26:545–556

    Article  PubMed  CAS  Google Scholar 

  • Renaut S, Nolte AW, Rogers SM, Derome N, Bernatchez L (2011) SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp). Mol Ecol 20:545–559. doi:10.1111/j.1365-294X.2010.04952.x

    Article  PubMed  Google Scholar 

  • Resende MDV et al (2012a) Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytol 194:116–128

    Article  PubMed  Google Scholar 

  • Resende MFR et al (2012b) Accelerating the domestication of trees using genomic selection: accuracy of prediction models across ages and environments. New Phytol 193:617–624

    Article  PubMed  Google Scholar 

  • Resende MFR et al (2012c) Accuracy of genomic selection methods in a standard dataset of loblolly pine (Pinus taeda L). Genetics 190:1503–1510

    Article  PubMed  PubMed Central  Google Scholar 

  • Richmond T (2000) Higher plant cellulose synthases. Genome Biol 1:reviews3001.3001 - reviews3001.3006

  • Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185

    Article  Google Scholar 

  • Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567. doi:10.1093/emboj/20.20.5556

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schindelman G et al (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schrader S, Sauter JJ (2002) Seasonal changes of sucrose-phosphate synthase and sucrose synthase activities in poplar wood (Populus x canadensis Moench robusta) and their possible role in carbohydrate metabolism. J Plant Physiol 159:833–843

    Article  CAS  Google Scholar 

  • Sexton TR et al (2012) Pectin methylesterase genes influence solid wood properties of eucalyptus pilularis. Plant Physiol 158:531–541. doi:10.1104/pp. 111.181602

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Spokevicius AV et al (2007) beta-tubulin affects cellulose microfibril orientation in plant secondary fibre cell walls. Plant J 51:717–726

    Article  PubMed  CAS  Google Scholar 

  • Stackpole DJ, Vaillancourt RE, Md A, Potts BM (2010a) Age trends in genetic parameters for growth and wood density in Eucalyptus globulus tree. Genet Genomes 6:179–193

    Article  Google Scholar 

  • Stackpole DJ, Vaillancourt RE, Alves A, Rodrigues J, Potts BM (2011) Genetic variation in the chemical components of eucalyptus globulus wood. G3 1:151–159. doi:10.1534/g3.111.000372

    Article  PubMed  PubMed Central  Google Scholar 

  • Stackpole DJ, Vaillancourt RE, Downes G, Harwood CE, Potts BM (2010b) Genetic control of kraft pulp yield in eucalyptus globulus Canadian. J Forest Res 40:917–927

    Article  Google Scholar 

  • Steane DA, Conod N, Jones RC, Vaillancourt RE, Potts BM (2006) A comparative analysis of population structure of a forest tree, Eucalyptus globulus (Myrtaceae), using microsatellite markers and quantitative traits. Tree Genet Genom 2:30–38

    Article  Google Scholar 

  • Steane DA et al (2011) Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping. Mol Phylogen Evol 59:206–224. doi:10.1016/j.ympev.2011.02.003

    Article  Google Scholar 

  • Stich B, Möhring J, Piepho H, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754

    Article  PubMed  PubMed Central  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies Proceedings of the National Academy of Sciences of the United States of America 100:9440–9445 doi:10.1073/pnas.1530509100

  • Stouffer SA, Suchman EA, De Vinney LC, Star SA, Williams RJ (1949) The American soldier: adjustment during army life. Princeton University, New Jersey

    Google Scholar 

  • Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    Article  PubMed  Google Scholar 

  • Szyjanowicz PMJ, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740

    Article  PubMed  CAS  Google Scholar 

  • Tchin BL, Ho WS, Pang SL, Ismail J (2011) Gene-associated single nucleotide polymorphism (SNP) in cinnamate 4-hydroxylase (C4H) and cinnamyl alcohol dehydrogenase (CAD) genes from acacia mangium superbulk trees. Biotechnology 10:303–315

    Article  CAS  Google Scholar 

  • Thavamanikumar S (2010) ‘Using genetic association studies for the improvement of wood and fibre properties in Eucalyptus globulus ssp. globulus Labill’ (PhD thesis). The University of Melbourne

  • Thavamanikumar S, McManus LJ, Tibbits JFG, Bossinger G (2011) The significance of single nucleotide polymorphisms (SNPs) in Eucalyptus globulus breeding programs. Aus For 74:23–29

    Article  Google Scholar 

  • Thavamanikumar S, Southerton S, Bossinger G, Thumma B (2013) Dissection of complex traits in forest trees—opportunities for marker-assisted selection. Tree Genet Genom 1–13 doi:10.1007/s11295-013-0594-z

  • Thavamanikumar S, Southerton S, Thumma B (2014) RNA-Seq using two populations reveals genes and alleles controlling wood traits and growth in eucalyptus nitens. PLoS ONE 9:e101104. doi:10.1371/journal.pone.0101104

    Article  PubMed  PubMed Central  Google Scholar 

  • Thumma BR, MacMillan CP, Southerton SG, Williams D, Joyce K, Ravenwood IC (2010) Accelerated breeding for high pulp yield in E. nitens using DNA markers identified in 100 cell wall genes: the hottest 100 (research report) forest and wood products. Australia Research Reports PNC052-0708

  • Thumma BR, Matheson BA, Zhang D, Meeske C, Meder R, Downes GM, Southerton SG (2009) Identification of a Cis-acting regulatory polymorphism in a eucalypt COBRA-like gene affecting cellulose content. Genetics 183:1153–1164

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Thumma BR, Nolan MR, Evans R, Moran GF (2005) Polymorphisms in cinnamoyl CoA reductase (CCR) are associated with variation in microfibril angle in eucalyptus spp. Genetics 171:1257–1265

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tibbits JFG, McManus LJ, Spokevicius AV, Bossinger G (2006) A rapid method for tissue collection and high-throughput isolation of genomic DNA from mature trees. Plant Mol Biol Rep 24:81–91

    Article  CAS  Google Scholar 

  • Traurig M et al (2009) Common variation in SIM1 is reproducibly associated with BMI in Pima Indians. Diabetes (New York) 58:1682–1689. doi:10.2337/db09-0028

    CAS  Google Scholar 

  • Vander Mijnsbrugge K, Meyermans H, Van Montagu M, Bauw G, Boerjan W (2000) Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210:589–598

    Article  PubMed  CAS  Google Scholar 

  • Washusen R (2002) Tension wood occurrence in eucalyptus globulus labill. II. The spatial distribution of tension wood and its association with stem form. Aust For 65:127–134

    Article  Google Scholar 

  • Xu SZ (2003) Theoretical basis of the Beavis effect. Genetics 165:2259–2268

    PubMed  PubMed Central  Google Scholar 

  • Yang J et al (2003) Novel gene expression profiles define the metabolic and physiological processes characteristic of wood and its extractive formation in a hardwood tree species Robinia pseudoacacia. Plant Mol Biol 52

  • Yang SS et al (2011) Using RNA-Seq for gene identification, polymorphism detection and transcript profiling in two alfalfa genotypes with divergent cell wall composition in stems. BMC Genomics 12:199

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yeoh SH, Bell JC, Foley WJ, Wallis IR, Moran GF (2012) Estimating population boundaries using regional and local-scale spatial genetic structure: an example in Eucalyptus globulus. Tree Genet Genom 8:695–708. doi:10.1007/s11295-011-0457-4

    Article  Google Scholar 

  • Yu JM et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  PubMed  CAS  Google Scholar 

  • Zhao J et al (2007a) Association mapping of leaf traits, flowering time, and phytate content in Brassica rapa. Genome 50:963–973

    Article  PubMed  CAS  Google Scholar 

  • Zhao KY et al (2007b) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4

    Article  PubMed  PubMed Central  Google Scholar 

  • Zollner S, Pritchard JK (2007) Overcoming the winner’s curse: estimating penetrance parameters from case–control data. Am J Hum Genet 80:605–615. doi:10.1086/512821

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zuo JR, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH (2000) KORRIGAN, an arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12:1137–1152

    PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

The authors wish to thank Gunns Ltd for providing access to the provenance-progeny trial to collect DNA samples and the Southern Tree Breeding Association for access to the validation population and provision of phenotypic data and breeding values. Dr. Chris Harwood is thanked for his constant support throughout the project and for comments on the manuscript. Professor Brad Potts and Dr. Pauline Garnier-Géré are thanked for their comments on the manuscript. Funding support for this project was provided by the CRC for Forestry (www.crcforestry.com.au).

Data archiving statement

Genotype (SNP) data and covariates (population structure and Kinship estimates) were submitted to the TreeGenes Database (http://dendrome.ucdavis.edu/treegenes/; accession number TGDR033). Phenotype data are commercial data and are archived in the Southern Tree Breeding Association (STBA) DataPlan database. These can be provided on request.

Author information

Authors and Affiliations

  1. Department of Forest and Ecosystem Science, The University of Melbourne, Water Street, Creswick, VIC, 3363, Australia

    Saravanan Thavamanikumar, Luke J. McManus, Peter K. Ades, Gerd Bossinger & Josquin F. G. Tibbits

  2. Co-operative Research Centre for Forestry, Private Bag 12, Hobart, TAS, 7001, Australia

    Saravanan Thavamanikumar, Luke J. McManus, Peter K. Ades, Gerd Bossinger, Desmond J. Stackpole, Sara Hadjigol, Jules S. Freeman, René E. Vaillancourt & Josquin F. G. Tibbits

  3. School of Plant Science, University of Tasmania, Private Bag 55, Hobart, TAS, 7001, Australia

    Desmond J. Stackpole, Sara Hadjigol, Jules S. Freeman & René E. Vaillancourt

  4. Plant Plan Genetics Pty Ltd, PO Box 1811, Mount Gambier, SA, 5290, Australia

    Richard Kerr

  5. CRN Research Fellow, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Locked Bag 4, Maroochydore, QLD, 4558, Australia

    Jules S. Freeman

  6. South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 10650, Guangdong, People’s Republic of China

    Peng Zhu

  7. CSIRO Agriculture Flagship, GPO Box 1600, Acton, Canberra, ACT, 2601, Australia

    Saravanan Thavamanikumar

  8. Department of Environment and Primary Industries, Biosciences Research Division, 5 Ring Road, Bundoora, Melbourne, VIC, 3083, Australia

    Josquin F. G. Tibbits

  9. PT Riau Andalan Pulp and Paper, Pangkalan Kerinci, Riau, Indonesia, 28300

    Desmond J. Stackpole

Authors
  1. Saravanan Thavamanikumar
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  2. Luke J. McManus
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  3. Peter K. Ades
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  4. Gerd Bossinger
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  5. Desmond J. Stackpole
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  6. Richard Kerr
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  7. Sara Hadjigol
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  8. Jules S. Freeman
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  9. René E. Vaillancourt
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  10. Peng Zhu
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  11. Josquin F. G. Tibbits
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Corresponding author

Correspondence to Josquin F. G. Tibbits.

Additional information

Communicated by D. Grattapaglia

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Thavamanikumar, S., McManus, L.J., Ades, P.K. et al. Association mapping for wood quality and growth traits in Eucalyptus globulus ssp. globulus Labill identifies nine stable marker-trait associations for seven traits. Tree Genetics & Genomes 10, 1661–1678 (2014). https://doi.org/10.1007/s11295-014-0787-0

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  • DOI: https://doi.org/10.1007/s11295-014-0787-0

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