Skip to main content
SpringerLink
Log in

Single-nucleotide polymorphisms in the 5′ UTR of UDP-glucose dehydrogenase (PtUGDH) associate with wood properties in Populus tomentosa

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Association studies have emerged as a powerful tool for identification of markers associated with quantitative traits in forest trees. The cytosolic enzyme uridine 5′ diphosphate-glucose dehydrogenase (UGDH) converts UDP-glucose to UDP-glucuronate and affects cell wall formation in higher plants. Here, we used association genetics to identify UDP-glucose dehydrogenase (PtUGDH) allelic variation that associates with wood quality traits in Populus tomentosa. We isolated a 1,828 bp PtUGDH cDNA encoding a polypeptide of 481 amino acids. Expression analysis revealed that PtUGDH was expressed predominantly in young root, developing xylem from vascular tissues, and young leaves, suggesting that UGDH functions in cell wall formation. We identified 59 single-nucleotide polymorphisms (SNPs; π T  = 0.00475) by resequencing the PtUGDH locus of 40 individuals and genotyped the 22 most common SNPs (minor allele frequency >10 %) in a discovery population (n = 426). Linkage disequilibrium (LD) analysis showed that LD did not extend over the entire gene (r 2 < 0.1, within 300 bp). Association studies indicated that three SNPs (false discovery rate, Q < 0.05) and 12 haplotypes (Q < 0.05) were significantly associated with wood properties. The three significant SNPs are all in the 5′ untranslated regions of PtUGDH, and the phenotypic variance explained by each SNP ranged from 5.37 to 11.97 %. We validated one association in a validation population (n = 1,200) and validated another association by examining its effect on gene expression. The present study provided molecular markers associated with fiber length and holocellulose content, markers that have potential applications in marker-assisted breeding.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abecasis GR, Ghosh D, Nichols TE (2005) Linkage disequilibrium: ancient history drives the new genetics. Hum Hered 59:118–124

    PubMed  Google Scholar 

  • Akey J, Jin L, Xiong M (2001) Haplotypes vs single marker linkage disequilibrium tests: what do we gain? Eur J Hum Genet 9(4):291–300

    Google Scholar 

  • Amidon TE (1981) Effect of the wood properties of hardwoods on kraft paper properties. Tappi 64:123–126

    CAS  Google Scholar 

  • Amino S, Takeuchi Y, Komamine A (1985) Changes in the enzyme activities involved in formation and inter-conversion of UDP-sugars during cell cycle in a synchronous culture of Catharanthus roseus. Physiol Plant 64:111–117

    CAS  Google Scholar 

  • Barrett LW, Fletcher S, Wilton SD (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 69:3613–3634

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beaulieu J, Doerksen T, Boyle B, Clement S, Deslauriers M et al (2011) Association genetics of wood physical traits in the conifer White Spruce and relationships with gene expression. Genetics 188:197–214

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    CAS  PubMed  Google Scholar 

  • Campbell RE, Sala RF, van de Rijn I, Tanner ME (1997) Properties and kinetic analysis of UDP-glucose dehydrogenase from group A Streptococci. J Biol Chem 272:3416–3422

    CAS  PubMed  Google Scholar 

  • Cave JD (1966) Theory of X-ray measurement of microfibril angle in wood. J For Prod 16:37–42

    Google Scholar 

  • Chanock SJ, Manolio T, Boehnke M, Boerwinkle E, Hunter DJ et al (2007) Replicating genotype–phenotype associations. Nature 447:655–660

    CAS  PubMed  Google Scholar 

  • Chhatre VE, Byam TD, Neale DB, Wegrzyn JL, Krutovsky KV (2013) Genetics structure and association mapping of adaptive and selective traits in the east Texas loblolly pine (Pinus taeda L.) breeding populations. Tree Genet Genomes. doi:10.1007/s11295-013-0624-x

    Google Scholar 

  • Chung BYW, Simons C, Firth AE, Brown CM, Hellens RP (2006) Effect of 5′ UTR introns on gene expression in Arabidopsis thaliana. BMC Genomics 7:120

    PubMed Central  PubMed  Google Scholar 

  • Collins FS, Guyer MS, Chakravarti A (1997) Variations on a theme: cataloging human DNA sequence variation. Science 279:1580–1581

    Google Scholar 

  • Curie C, Liboz T, Bardet C, Gander E, Medale C et al (1991) Cis and trans-acting elements involved in the activation of Arabidopsis thaliana A1 gene encoding the translation elongation factor EF-1 alpha. Nucleic Acids Res 19:1305–1310

    CAS  PubMed Central  PubMed  Google Scholar 

  • Curie C, Liboz T, Montane MH, Rouan D, Axelos M et al (1992) The activation process of Arabidopsis thaliana A1 gene encoding the translation elongation factor EF-1 alpha is conserved among angiosperms. Plant Mol Biol 18:1083–1089

    CAS  PubMed  Google Scholar 

  • Curie C, Axelos M, Bardet C, Atanassova R, Chaubet N et al (1993) Modular organization and development activity of an Arabidopsis thaliana EF-1 alpha gene promoter. Mol Gen Genet 238:428–436

    CAS  PubMed  Google Scholar 

  • Denis M, Favreau B, Ueno S, Camus-Kulandaivelu L, Chaix G, Gion JM, Nourrisier-Mountou S, Polidori J, Bouvet JM (2013) Genetics variation of wood chemical traits and association with underlying genes in Eucalyptus urophylla. Tree Genet Genomes 9:927–942

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dillon SK, Brawner JT, Meder R, Lee DJ, Southerton SG (2012) Association genetics in Corymbia citriodora subsp. Variegate identifies single nucleotide polymorphisms affecting wood growth and cellulosic pulp yield. New Phytol 195:596–608

    CAS  PubMed  Google Scholar 

  • Djerbi S, Aspeborg H, Nilsson P, Sundberg B, Mellerowicz E, Blomqvist K, Teeri TT (2004) Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.) × P. tremuloides (Michx.). Cellulose 11:301–312

    CAS  Google Scholar 

  • Du QZ, Wang BW, Wei ZZ, Zhang DQ, Li BL (2012) Genetic diversity and population structure of Chinese white poplar (Populus tomentosa) revealed by SSR markers. J Hered 103:853–862

    PubMed  Google Scholar 

  • Du QZ, Pan W, Xu BH, Li BL, Zhang DQ (2013) Polymorphic simple sequence repeat (SSR) loci within cellulose synthase (PtoCesA) genes are associated with growth and wood properties in Populus tomentosa. New Phytol 197:763–776

    CAS  PubMed  Google Scholar 

  • Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD et al (2009) Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold hardiness related traits. Genetics 182:1289–1302

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ericson MC, Elbein AD (1980) The biochemistry of plants. Academic, New York, pp 589–616

    Google Scholar 

  • Feingold DS, Barber GA (1990) Methods in plant biochemistry. Academic, London, pp 39–78

    Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    CAS  PubMed  Google Scholar 

  • Gibeaut DM (2000) Nucleotide sugars and glucosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol Biochem 38:69–80

    CAS  Google Scholar 

  • Gibeaut DM, Carpita NC (1994) Biosynthesis of plant cell wall polysaccharides. FASEB J 8:904–915

    CAS  PubMed  Google Scholar 

  • Gordon D, Finch SJ (2005) Factors affecting statistical power in the detection of genetic association. J Clin Invest 115:1408–1418

    CAS  PubMed Central  PubMed  Google Scholar 

  • Greene CS, Penrod NM, Williams SM, Moore JH (2009) Failure to replicate a genetic association may provide important clues about genetic architecture. PLoS ONE 4:e5639

    PubMed Central  PubMed  Google Scholar 

  • Guerra FP, Wegrzyn JL, Sykes R, Davis MF, Stanton BJ, Neale DB (2013) Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol 197:162–176

    CAS  PubMed  Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    CAS  PubMed  Google Scholar 

  • Hall D, Tegström C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 9:157–165

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Hedrick PW (1987) Gametic disequilibrium measures: proceed with caution. Genetics 117:331–341

    CAS  PubMed Central  PubMed  Google Scholar 

  • Henderson CR (1975) Best linear unbiased estimation and prediction under a selection model. Biometrics 31:423–447

    CAS  PubMed  Google Scholar 

  • Higuchi T (1997) Biochemistry and molecular biology of wood. Springer, London

    Google Scholar 

  • Hir HL, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220

    PubMed  Google Scholar 

  • Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:45–61

    Google Scholar 

  • Hong X, Scofield DG, Lynch M (2006) Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol 23(12):2392–2404

    CAS  PubMed  Google Scholar 

  • Horn RA (1978) Morphology of pulp fiber from hardwoods and influence on paper strength. USDA For Serv Res Pap FPL 312, For Prod Lab, Madison, WI, USA

  • Huang ZH (1992) The study on the climatic regionalization of the distributional region of Populus tomentosa. Journal of Beijing Forestry University 14:26–32

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ingvarsson PK, Street NR (2010) Association genetics of complex traits in plants. New Phytol 189:909–922

    PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johansson H, Sterky F, Amini B (2002) Molecular cloning and characterization of a cDNA encoding poplar UDP- glucose dehydrogenase, a key gene of hemicellulose/pectin formation. Biochim Biophys Acta 1576:53–58

    CAS  PubMed  Google Scholar 

  • Kamo K, Kim AY, Park SH, Joung YH (2012) The 5′ UTR-intron of the Gladiolus polyubiquitin promoter GUBQ1 enhances translation efficiency in Gladiolus and Arabidopsis. BMC Plant Biol 12:79

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim MY, Ha BK, Jun TH, Hwang EY, Van K et al (2004) Single nucleotide polymorphism discovery and linkage mapping of lipoxygenase-2 gene (Lx2) in soybean. Euphytica 135:169–177

    CAS  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172

    CAS  PubMed  Google Scholar 

  • Koshkin AA, Rajwanshi VK, Wengel J (1998a) Novel convenient syntheses of LNA [2.2.1] bicyclonucleosides. Tetrahedron Lett 39:4381–4384

    CAS  Google Scholar 

  • Koshkin AA, Singh SK, Nielsen P, Rajwanshi VK, Kumar R et al (1998b) LNA (locked nucleic acids): synthesis of the adenine, cytosine, guanine, 5-methylcytosine, thymine and uracil bicyclonucleoside monomers, oligo merisation, and unprecendented nucleic acid recognition. Tetrahedron 54:3607–3630

    CAS  Google Scholar 

  • Külheim C, Yeoh SH, Maintz J, Foley WJ, Moran GF (2009) Comparative SNP diversity among four Eucalyptus species for genes from secondary metabolite biosynthetic pathways. BMC Genomics 10:1–11

    Google Scholar 

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

    Google Scholar 

  • Li MA (2009) The effect of exogenous NAA on photoassimilate reallocation of poplar. Dissertation, Nanjing Forestry University

  • Liang H, Yu FG (2007) Effects of N-1-naphthylphthalamic acid an exogenous IAA and GA3 on the elongation and gravitropic responses of Arabidopsis roots. Plant Physiol Communications 43:653–656

    Google Scholar 

  • Liepman AH, Wightman R, Geshi N, Turner SR, Scheller HV (2010) Arabidopsis—a powerful model system for plant cell wall research. Plant J 61:1107–1121

    CAS  PubMed  Google Scholar 

  • Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA et al (2009) Finding the missing heritability of complex diseases. Nature 461:747–753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300

    CAS  PubMed  Google Scholar 

  • Meylan BA (1967) Measurement of microfibril angle by X-ray diffraction. For Prod J 17:51–58

    Google Scholar 

  • Migneault S, Koubaa A, Erchiqui F, Chaala A, Englund K et al (2008) Effect of fiber length on processing and properties of extruded wood-fiber/HDPE composites. J Appl Polym Sci 110:1085–1092

    CAS  Google Scholar 

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122

    CAS  PubMed  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330

    CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nelsetuen GL, Kirkwood S (1971) The mechanism of action of uridine diphosphoglucose dehydrogenase. J Biol Chem 246:3828–3834

    Google Scholar 

  • Pang T, Guo LL, Xia XL, Yin WL (2012) Effects of 5′ UTR intron of AmCBL1 gene in a xerophyte Ammopiptanthus mongolicus. Journal of Beijing Forestry University 33:157–165

    Google Scholar 

  • Pesole G, Grillo G, Larizza A, Liuni S (2000) The untranslated regions of eukaryotic mRNAs: structure, function, evolution and bioinformatic tools for their analysis. Brief Bioinform 1:223–249

    Google Scholar 

  • Petit JR, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Evol Syst 37:187–214

    Google Scholar 

  • Porth I, Klápště J, Skyba O, Lai BS, Geraldes A et al (2013) Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control, and genetic correlations. New Phytol 197:777–790

    CAS  PubMed  Google Scholar 

  • Purcell S, Cherny SS, Sham PC (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19:149–150

    CAS  PubMed  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR et al (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A 98:11479–11484

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ringner M, Krogh M (2005) Folding free energies of 5′-UTRs impact post-transcriptional regulation on a genomic scale in yeast. PLoS Comput Biol 1:e72

    PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Robertson D, Smith C, Bolwell GP (1996) Inducible UDP-glucose dehydrogenase from French bean (Phaseolus vulgaris L.) locates to vascular tissue and has alcohol dehydrogenase activity. Biochem J 313:311–317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rose AB (2004) The effect of intron location on intron-mediated enhancement of gene expression in Arabidopsis. Plant J 40:744–751

    CAS  PubMed  Google Scholar 

  • Rose AB, Beliakoff JA (2000) Intron-mediated enhancement of gene expression independent of unique intron sequences and splicing. Plant Physiol 122:535–542

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    CAS  PubMed  Google Scholar 

  • Rubery PH (1972) The activity of uridine diphosphate-d-glucose nicotinamide–adenine dinucleotide oxidoreductase in cambial tissue and differentiating xylem isolated from sycamore trees. Planta 103:188–192

    CAS  PubMed  Google Scholar 

  • Samac DA, Litterer L, Temple G, Jung H, Somers DA (2004) Expression of UDP-glucose dehydrogenase reduces cell-wall polysaccharide concentration and increases xylose content in alfalfa stems. Appl Biochem Biotech 113–116:1167–1182

    Google Scholar 

  • Samadder P, Sivamani E, Lu JL, Li XG, Qu RD (2008) Transcriptional and post-transcriptional enhancement of gene expression by the 5′ UTR intron of rice rubi3 gene in transgenic rice cells. Mol Genet Genomics 279:429–439

    CAS  PubMed  Google Scholar 

  • Schiller JG, Lamy F, Frazier R, Feingold DS (1976) UDP-glucose dehydrogenase from Escherichia coli: purification and subunit structure. Biochim Biophys Acta 453:418–425

    CAS  PubMed  Google Scholar 

  • Schimleck LR, Kube PS, Raymond CA (2004) Genetic improvement of kraft pulp yield in Eucalyptus nitens using cellulose content determined by near infrared spectroscopy. Can J For Res 34:2363–2370

    CAS  Google Scholar 

  • Seitz B, Klos C, Wurm M, Tenhaken R (2000) Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns. Plant J 21:537–546

    CAS  PubMed  Google Scholar 

  • Serapiglia MJ, Cameron KD, Stipanovic AJ, Smart LB (2012) Correlations of expression of cell wall biosynthesis genes with variation in biomass composition in shrub willow (Salix spp.) biomass crops. Tree Genet Genomes 8:775–788

    Google Scholar 

  • Southerton SG, MacMillan CP, Bell JC, Bhuiyan N, Downes G et al (2010) Association of allelic variation in xylem genes with wood properties in Eucalyptus nitens. Austral For 73:259–264

    Google Scholar 

  • Stewart DC, Copeland L (1998) Uridine 5 V-diphosphate-glucose dehydrogenase from soybean nodules. Plant Physiol 116:349–355

    CAS  PubMed Central  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc Ser B 64:479–498

    Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci U S A 100:9440–9445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. J Roy Stat Soc Ser B 66:187–205

    Google Scholar 

  • Sun HY (2008) The regulative effects of exogenous ABA and Ca2+ on the growth of poplar cuttings. Dissertation, Nanjing Forestry University

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    CAS  PubMed  Google Scholar 

  • Tang L, Kwon SY, Kim SH, Kim JS, Choi JS, Cho KY, Sung CK, Kwak SS, Lee HS (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380–1386

    CAS  PubMed  Google Scholar 

  • Tenhaken R, Thulke O (1996) Cloning of an enzyme that synthesizes a key nucleotide-sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase. Plant Physiol 112:1127–1134

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thireos G, Penn MD, Greer H (1984) 5′ untranslated sequences are required for the translational control of a yeast regulatory gene. Proc Natl Acad Sci U S A 81:5096–5100

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tian JX, Du QZ, Chang MQ, Zhang DQ (2012) Allelic variation in PtGA20Ox associates with growth and wood properties in Populus spp. PLoS ONE 7(12):e53116

    CAS  PubMed Central  PubMed  Google Scholar 

  • Voight BF, Pritchard JK (2005) Confounding from cryptic relatedness in case-control association studies. PLoS Genet 1(3):e32. doi:10.1371/journal.pgen.0010032

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:188–193

    Google Scholar 

  • Wegrzyn JL, Eckert AJ, Choi M, Lee JM, Stanton BJ et al (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532

    CAS  PubMed  Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer, Sunderland

    Google Scholar 

  • Wilkie GS, Dickson KS, Gray NK (2003) Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28:182–188

    CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signaling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    CAS  PubMed  Google Scholar 

  • Witt HJ (1992) UDP-glucose metabolism during differentiation and dedifferentiation of Riella helicophylla. J Plant Physiol 140:276–281

    CAS  Google Scholar 

  • Wullschleger SD, Yin TM, DiFazio SP, Tschaplinski TJ, Gunter LE et al (2005) Phenotypic variation in growth and biomass distribution for two advanced-generation pedigrees of hybrid poplar. Can J For Res 35:1779–1789

    CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang XH, Liang Z, Lu CM (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 138:2299–2309

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu MX (2009) The effects of gibberellic acid on photoassimilate reallocation pattern of the poplar cutting seeding. Dissertation, Nanjing Forestry University

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    CAS  PubMed  Google Scholar 

  • Zaykin DV, Westfall PH, Young SS, Karnoub MA, Wagner MJ, Ehm MG (2002) Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Hum Hered 53:79–91

    PubMed  Google Scholar 

  • Zhang DQ, Zhang ZY, Yang K, Li BL (2004) Genetic mapping in (Populus tomentosa × P. bolleana) and P. tomentosa Carr. using AFLP markers. Theor Appl Genet 108(4):657–662

    CAS  PubMed  Google Scholar 

  • Zhang DQ, Zhang ZY, Yang K (2006) QTL analysis of growth and wood chemical content traits in an interspecific backcross family of white poplar (Populus tomentosa × P. bolleana) × P. tomentosa. Can J For Res 36:2015–2023

    CAS  Google Scholar 

  • Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li BL (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    CAS  PubMed  Google Scholar 

  • Zhang DQ, Xu BH, Yang XH, Zhang ZY, Li BL (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genet Genomes 7:443–456

    Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National “863” Plan Project (no. 2011AA10020102), the State Key Basic Research Program of China (no. 2012CB114506), and the Project of the National Natural Science Foundation of China (nos. 31170622 and 30872042).

Data archiving statement

Sequence data from this article have been deposited with the GenBank Data Library under the accession nos. KC329533–KC329573.

Author information

Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Jiaxing Tian, Qingzhang Du, Bailian Li & Deqiang Zhang

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Jiaxing Tian, Qingzhang Du, Bailian Li & Deqiang Zhang

Authors
  1. Jiaxing Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qingzhang Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bailian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deqiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deqiang Zhang.

Additional information

Communicated by P. Ingvarsson

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

DOC 30 kb

ESM 2

DOC 30 kb

ESM 3

DOC 50 kb

ESM 4

DOC 198 kb

ESM 5

DOC 52 kb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tian, J., Du, Q., Li, B. et al. Single-nucleotide polymorphisms in the 5′ UTR of UDP-glucose dehydrogenase (PtUGDH) associate with wood properties in Populus tomentosa . Tree Genetics & Genomes 10, 339–354 (2014). https://doi.org/10.1007/s11295-013-0689-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-013-0689-6

Keywords

Search

Navigation