Skip to main content
Log in

Genome-wide association studies of bark texture in Populus trichocarpa

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

A Correction to this article was published on 29 November 2019

This article has been updated

Abstract

Plants have developed bark as a defense barrier to deal with environmental stresses, such as pathogen invasion, drought, and UV radiation. Bark is composed of dead differentiated cells and is formed when radial expansion pushes the cortex and epidermis outward creating secondary meristem. However, the genetic control of this complex phenotype is generally unknown. Here, we use association mapping to define the genomic regions associated with natural variation in bark texture (BT) in Populus trichocarpa. Clonally replicated provenance trials of P. trichocarpa were studied for BT collected across three sites, multiple years, and (2–3) biological replicates per site. Forty-one genomic intervals containing SNPs significantly associated with BT were detected that were highly reproducible across sites, years, and replicates. A list of candidate genes within these regions with related putative function was identified. A total of 98 genes were considered candidate genes due to significance and putative function with connection to the phenotype. Association mapping using low coverage sequencing allowed us to detect narrow genomic intervals (1–20 kb) with high reproducibility and shared candidate genes. For example, a membrane-associated apoptosis protein and a wall-associated receptor kinase (PR5K-like) protein, which both are involved in radial growth and tissue differentiation, lie within significant trait-associated region. Two copies of root hair defective3 genes, transmembrane protein in Populus differentiating xylem and phloem, were also significantly associated with BT and co-located with major quantitative trait locus (QTL) for BT, bark thickness, and diameter from our previous study suggesting an important role in radial growth.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Change history

  • 29 November 2019

    The co-author Jin Zhang was unintentionally forgotten on the original author list. The correct Author list is presented in this paper.

Abbreviations

GWAS:

genome-wide association study

BT:

bark texture

QTL:

quantitative trait loci

LG:

linkage group

CLA:

Clatskanie site

COR:

Corvallis site

PLC:

Placerville sites

FDR:

false discovery rate

EMMA:

efficient mixed model association

LD:

linkage disequilibrium

References

  • Addicott FT (1982) Abscission. Univ of California Press, Berkeley

    Google Scholar 

  • Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  CAS  Google Scholar 

  • Asif M, al-Mansoub MA, Khan MDSS, Yehya AHS, Ezzat MO, Oon CE, Atif M, Abdul Majid AS, Abdul Majid AMS (2017) Molecular mechanisms responsible for programmed cell death-inducing attributes of terpenes from Mesua ferrea stem bark towards human colorectal carcinoma HCT 116 cells. J Appl Biomed 15:71–80

    Article  Google Scholar 

  • Bachmair A, Becker F, Masterson R, Schell J (1990) Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J 9:4543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265

    Article  CAS  PubMed  Google Scholar 

  • Bdeir R, Muchero W, Yordanov Y, Tuskan GA, Busov V, Gailing O (2017) Quantitative trait locus mapping of Populus bark features and stem diameter. BMC Plant Biol 17:224

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beaver R, Wilding N, Collins N, Hammond P, Webber J (1989) Insect-fungus relationships in the bark and ambrosia beetles. Insect-fungus interactions:121–143

  • Bent AF (1996) Plant disease resistance genes: function meets structure. Plant Cell 8:1757–1771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6:e1000940

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brembu T, Winge P, Seem M, Bones AM (2004) NAPP and PIRP encode subunits of a putative wave regulatory protein complex involved in plant cell morphogenesis. Plant Cell 16:2335–2349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351

    Article  PubMed  CAS  Google Scholar 

  • Caño-Delgado A, Lee J-Y, Demura T (2010) Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu Rev Cell Dev Biol 26:605–637

    Article  PubMed  CAS  Google Scholar 

  • Carlquist S (1996) Wood, bark, and stem anatomy of Gnetales: a summary. Int J Plant Sci 157:S58–S76

    Article  Google Scholar 

  • Carpita N, Tierney M, Campbell M (2001) Molecular biology of the plant cell wall: searching for the genes that define structure, architecture and dynamics. Plant Mol Biol 47:1–5

    Article  CAS  PubMed  Google Scholar 

  • Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114:594–600

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Fan B, Du L, Chen Z (2004) Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis. Plant Mol Biol 56:271–283

    Article  CAS  PubMed  Google Scholar 

  • Climent J, Tapias R, Pardos JA, Gil L (2004) Fire adaptations in the Canary Islands pine (Pinus canariensis). Plant Ecol 171:185–196

    Article  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Biol 49:427–451

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321

    Article  CAS  PubMed  Google Scholar 

  • Deeks MJ, Kaloriti D, Davies B, Malhó R, Hussey PJ (2004) Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol 14:1410–1414

    Article  CAS  PubMed  Google Scholar 

  • Evans LM, Slavov GT, Rodgers-Melnick E, Martin J, Ranjan P, Muchero W, Brunner AM, Schackwitz W, Gunter L, Chen JG, Tuskan GA, DiFazio SP (2014) Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nat Genet 46:1089–1096

    Article  CAS  PubMed  Google Scholar 

  • Fitch R (2006) WinSTAT for Excel. The statistics add-in for Microsoft Excel R Fitch Software

  • Fossdal CG, Yaqoob N, Krokene P, Kvaalen H, Solheim H, Yakovlev IA (2012) Local and systemic changes in expression of resistance genes, nb-lrr genes and their putative microRNAs in Norway spruce after wounding and inoculation with the pathogen Ceratocystis polonica. BMC Plant Biol 12:105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franciosini A, Lombardi B, Iafrate S, Pecce V, Mele G, Lupacchini L, Rinaldi G, Kondou Y, Gusmaroli G, Aki S, Tsuge T, Deng XW, Matsui M, Vittorioso P, Costantino P, Serino G (2013) The Arabidopsis COP9 SIGNALOSOME INTERACTING F-BOX KELCH 1 protein forms an SCF ubiquitin ligase and regulates hypocotyl elongation. Mol Plant 6:1616–1629

    Article  CAS  PubMed  Google Scholar 

  • Gill A, Ashton D (1968) The role of bark type in relative tolerance to fire of three central Victorian eucalypts. Aust J Bot 16:491–498

    Article  Google Scholar 

  • Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567

    Article  CAS  PubMed  Google Scholar 

  • Grant EH, Fujino T, Beers EP, Brunner AM (2010) Characterization of NAC domain transcription factors implicated in control of vascular cell differentiation in Arabidopsis and Populus. Planta 232:337–352

    Article  CAS  PubMed  Google Scholar 

  • Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119:375–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhlen M, Teeri TT, Lundeberg J, Sundberg B, Nilsson P, Sandberg G (2001) A transcriptional roadmap to wood formation. Proc Natl Acad Sci 98:14732–14737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222–226

    Article  CAS  PubMed  Google Scholar 

  • Jelonek T, Pazdrowski W, Tomczak A, Arasimowicz-Jelonek M (2017) Lignification markers of the tracheid walls of scots pine (Pinus sylvestris (L.)) in various forms of dead bark. BioResources 12:3992–4003

    Article  CAS  Google Scholar 

  • Kang HM, Sul JH, Zaitlen NA, Kong S-y, Freimer NB, Sabatti C, Eskin E (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42:348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelleher CT, Chiu R, Shin H, Bosdet IE, Krzywinski MI, Fjell CD, Wilkin J, Yin T, DiFazio SP, Ali J (2007) A physical map of the highly heterozygous Populus genome: integration with the genome sequence and genetic map and analysis of haplotype variation. Plant J 50:1063–1078

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636

    Article  CAS  PubMed  Google Scholar 

  • Lafarguette F, Leplé JC, Déjardin A, Laurans F, Costa G, Lesage-Descauses MC, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phytol 164:107–121

    Article  CAS  PubMed  Google Scholar 

  • Lawes MJ, Adie H, Russell-Smith J, Murphy B, Midgley JJ (2011) How do small savanna trees avoid stem mortality by fire? The roles of stem diameter, height and bark thickness. Ecosphere 2:1–13

    Article  Google Scholar 

  • Legay S, Guerriero G, Deleruelle A, Lateur M, Evers D, André CM, Hausman J-F (2015) Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall. Plant Mol Biol 88:21–40

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Jin F, Chao Q, Wang B-C (2017) Proteomics analysis reveals the molecular mechanism underlying the transition from primary to secondary growth of poplar. J Plant Physiol 213:1–15

    Article  PubMed  CAS  Google Scholar 

  • Manenti G, Galvan A, Pettinicchio A, Trincucci G, Spada E, Zolin A, Milani S, Gonzalez-Neira A, Dragani TA (2009) Mouse genome-wide association mapping needs linkage analysis to avoid false-positive loci. PLoS Genet 5:e1000331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marshall JM, Smith EL, Mech R, Storer AJ (2013) Estimates of Agrilus planipennis infestation rates and potential survival of ash. Am Midl Nat 169:179–193

    Article  Google Scholar 

  • McCarthy RL et al (2010) The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant Cell Physiol 51:1084–1090

    Article  CAS  PubMed  Google Scholar 

  • McIntyre LM, Martin ER, Simonsen KL, Kaplan NL (2000) Circumventing multiple testing: a multilocus Monte Carlo approach to testing for association. Genet Epidemiol 19:18–29

    Article  CAS  PubMed  Google Scholar 

  • Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol Report 47:239–274

  • Meyer K, Shirley AM, Cusumano JC, Bell-Lelong DA, Chapple C (1998) Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc Natl Acad Sci 95:6619–6623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muchero W, Guo J, DiFazio SP, Chen JG, Ranjan P, Slavov GT, Gunter LE, Jawdy S, Bryan AC, Sykes R, Ziebell A, Klápště J, Porth I, Skyba O, Unda F, el-Kassaby YA, Douglas CJ, Mansfield SD, Martin J, Schackwitz W, Evans LM, Czarnecki O, Tuskan GA (2015) High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus. BMC Genomics 16:24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pausas JG (2015) Bark thickness and fire regime. Funct Ecol 29:315–327

    Article  Google Scholar 

  • Piquemal J, Lapierre C, Myton K, O’connell A, Schuch W, Grima-pettenati J, Boudet AM (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13:71–83

    Article  CAS  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127:1513–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246

    Article  CAS  PubMed  Google Scholar 

  • Rains MK, de Silva G, Dilini N, Molina I (2018) Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol 38:340–361

    Article  CAS  Google Scholar 

  • Romero C (2006) Tree responses to stem damage. PhD thesis. University of Florida, Gainsville, USA

  • Sengupta G, Palit P (2004) Characterization of a lignified secondary phloem fibre-deficient mutant of jute (Corchorus capsularis). Ann Bot 93:211–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, Gunter LE, Ranjan P, Vining K, Pomraning KR, Wilhelm LJ, Pellegrini M, Mockler TC, Freitag M, Geraldes A, el-Kassaby YA, Mansfield SD, Cronk QCB, Douglas CJ, Strauss SH, Rokhsar D, Tuskan GA (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725

    Article  CAS  PubMed  Google Scholar 

  • Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song D, Xi W, Shen J, Bi T, Li L (2011) Characterization of the plasma membrane proteins and receptor-like kinases associated with secondary vascular differentiation in poplar. Plant Mol Biol 76:97–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Bhalerao R, Larsson M, Villarroel R, van Montagu M, Sandberg G, Olsson O, Teeri TT, Boerjan W, Gustafsson P, Uhlen M, Sundberg B, Lundeberg J (1998) Gene discovery in the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags. Proc Natl Acad Sci 95:13330–13335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182

    Article  CAS  PubMed  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, Takken FL (2008) Structure–function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397

    Article  PubMed  CAS  Google Scholar 

  • Venkatesan T, Choi Y-W, Mun S-P, Kim Y-K (2016) Pinus radiata bark extract induces caspase-independent apoptosis-like cell death in MCF-7 human breast cancer cells. Cell Biol Toxicol 32:451–464

    Article  PubMed  Google Scholar 

  • Wang X, Zafian P, Choudhary M, Lawton M (1996) The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc Natl Acad Sci 93:2598–2602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Jiang C, Wang C, Yang Y, Yang L, Gao X, Zhang H (2014) Antisense expression of the fasciclin-like arabinogalactan protein FLA6 gene in Populus inhibits expression of its homologous genes and alters stem biomechanics and cell wall composition in transgenic trees. J Exp Bot 66:1291–1302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whitmore T (1962) Studies in systematic bark morphology. New Phytol 61:191–207

    Article  Google Scholar 

  • Xu P, Cai X-T, Wang Y, Xing L, Chen Q, Xiang C-B (2014) HDG11 upregulates cell-wall-loosening protein genes to promote root elongation in Arabidopsis. J Exp Bot 65:4285–4295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17:2314–2326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Yang Y, Zheng K, Xie M, Feng K, Jawdy SS, Gunter LE, Ranjan P, Singan VR, Engle N, Lindquist E, Barry K, Schmutz J, Zhao N, Tschaplinski TJ, LeBoldus J, Tuskan GA, Chen JG, Muchero W (2018) Genome-wide association studies and expression-based quantitative trait loci analyses reveal roles of HCT 2 in caffeoylquinic acid biosynthesis and its regulation by defense-responsive transcription factors in Populus. New Phytol 220:502–516

    Article  CAS  Google Scholar 

  • Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Sun J, Xu P, Zhang R, Li L (2014) Intron-mediated alternative splicing of Wood-ASSOCIATED NAC TRANSCRIPTION FACTOR1B regulates cell wall thickening during fiber development in Populus species. Plant Physiol 164:765–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Lee C, Zhong R, Ye Z-H (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Data archiving statement

Whole-genome resequencing, SNP/indel calling, and SnpEff analysis for the 544 individuals of this Populus GWAS population was previously described by Evans et al. (2014). In this study, we used the same sequencing and analytical pipelines to incorporate an additional 373 accessions (altogether 917 accessions). Briefly, reads were aligned to the P. trichocarpa reference genome version 3 using BWA 0.5.9-r16 with default parameters and SNPs and indels were called using SAMtools mpileup (-E –C 50 –DS –m 2 –F 0.000911 –d 50000) and bcftools (-bcgv –p 0.999089). The resulting SNP and indel dataset is available at http://bioenergycenter.org/besc/gwas/. The resulting SNP and indel dataset is available at http://bioenergycenter.org/besc/gwas/. To assess genetic control, we used the EMMA algorithm in the EMMAX software with kinship as the correction factor for genetic background effects (Zhou and Stephens 2012) to compute genotype to phenotype associations using 8.253,066 SNP variants with minor allele frequencies > 0.05 identified from whole-genome resequencing. Linkage disequilibrium (LD) was determined using HAPLOVIEW v.4.2 (Barrett et al. 2005). To account for multiple testing, we used the Bonferroni correction and considered as significant only those SNPs for which P < 0.05/8253066 = 6.06910−9. This correction is known to be conservative and thus “overcorrected” the raw P values (McIntyre et al. 2000).

Funding

Support for the phenotyping and graduate support for Roba Bdeir was provided by the USDA-NIFA grant (# 2012-67013-19389) to VB, YY, and OG. Additional partial support for Roba Bdeir was provided by the National Science Foundation grant to OG (# 1230803) as part of the “Sustainable Forest-Based Biofuel Pathways to Hydrocarbon Transportation Fuels” project at Michigan Tech. The Center for Bioenergy Innovation is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. This work was supported by the U.S. Department of Energy under Contract to Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the US Department of Energy under contract number DE-AC05-00OR22725. We also acknowledge support from the German Research Foundation (DFG) and the Open Access Publication Funds of Göttingen University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Oliver Gailing.

Additional information

Communicated by P. Ingvarsson

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Online Resource 1

Bark texture scale from smooth (1), medium flaky (2) to rough flaky (3) for the P. trichocarpa populations. (DOCX 395 kb)

Online Resource 2

Spearman’s rank correlation coefficients for bark texture phenotypes across five datasets (DOCX 18 kb)

Online Resource 3

Frequency distribution for bark texture across Clatskanie (CLA), Corvallis (COR) and Placerville (PLC) sites and various years (a, b, c, respectively). (DOCX 228 kb)

Online Resource 4

All 1825 SNPs associated with bark texture and the underlying genes within a 6 kb interval. The population in which these SNP were detected in, their position, linkage group and significance score along with the physical localization, annotation and expression profiles of the underlying genes are summarized. (XLSX 87 kb)

Online Resource 5

The 50 genomic regions most strongly associated with bark texture and the underlying genes. The population in which these 129 individual SNPs were detected, position, linkage group and significance score as well as the physical localization and annotation of the underlying genes are summarized. SNPs are categorized into three groups: reproducible across sites, reproducible within a site and reproducible but no putative gene detected within 50 kb interval. Scores of -log10 P > 6 are in bold, genes with SNPs within its genomic sequence are highlighted in yellow. (XLSX 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bdeir, R., Muchero, W., Yordanov, Y. et al. Genome-wide association studies of bark texture in Populus trichocarpa. Tree Genetics & Genomes 15, 14 (2019). https://doi.org/10.1007/s11295-019-1320-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-019-1320-2

Keywords

Profiles

  1. Roba Bdeir
  2. Oliver Gailing