Skip to main content

Advertisement

SpringerLink
Log in

A candidate gene-based association study reveals SNPs significantly associated with bud burst in European beech (Fagus sylvatica L.)

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

Abstract

European beech (Fagus sylvatica L.) is one of the most important deciduous forest tree species in Central Europe. Nevertheless, its adaptation potential to climate change is controversially discussed, and little is known about the molecular basis of climate change-relevant traits like bud burst. Here, we directly observed bud burst of beech seedlings originating from six different populations in Northern Germany in a large translocation experiment comprising 3600 individuals in three consecutive years. We genotyped more than 1200 individuals from the translocation experiment using 46 different SNP markers previously identified in candidate genes for bud burst. Association and outlier analyses were conducted to identify potentially adaptive SNPs. We found 10 SNPs significantly associated with bud burst in at least one analyzed year and five outlier SNPs potentially under directional selection. One SNP located in a histone gene was simultaneously revealed by both association and outlier analyses. This SNP might have the highest probability of being involved in the expression of bud burst.

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

Similar content being viewed by others

References

  • Ammer C, Albrecht L, Borchert H, Brosinger F, Dittmar C, Elling W, Ewald J, Felbermeier B, Hv G, Huss J, Kenk G, Kölling C, Kohnle U, Meyer P, Mosandl R, Moosmayer H-U, Palmer S, Reif A, Rehfuess K-E, Stimm B (2005) Zur Zukunft der Buche (Fagus sylvatica L.) in Mitteleuropa, Kritische Anmerkungen zu einem Beitrag von Rennenberg et al. (2004). All Forst-u J-Ztg 176:60–67

    Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira LG (2008) LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 9:323. doi:10.1186/1471-2105-9-323

    Article  PubMed Central  PubMed  Google Scholar 

  • Asuka Y, Tani N, Tsumura Y, Tomaru N (2004) Development and characterization of microsatellite markers for Fagus crenata Blume. Mol Ecol Notes 4:101–103. doi:10.1046/j.1471-8286.2003.00583.x

    Article  CAS  Google Scholar 

  • Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525. doi:10.1093/treephys/23.8.517

    Article  PubMed  Google Scholar 

  • Balding DJ (2006) A tutorial on statistical methods for population association studies. Nat Rev Genet 7:781–791. doi:10.1038/nrg1916

    Article  CAS  PubMed  Google Scholar 

  • Barrett RDH, Hoekstra HE (2011) Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12:767–80. doi:10.1038/nrg3015

    Article  CAS  PubMed  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. P Roy Soc B-Biol Sci 263:1619–1626. doi:10.1098/rspb.1996.0237

    Article  Google Scholar 

  • Bilela S, Dounavi A, Fussi B, Konnert M, Holst J, Mayer H, Rennenberg H, Simon J (2012) Natural regeneration of Fagus sylvatica L. adapts with maturation to warmer and drier microclimatic conditions. Forest Ecol Manag 275:60–67. doi:10.1016/j.foreco.2012.03.009

    Article  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss 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  CAS  PubMed  Google Scholar 

  • Capon F, Allen MH, Ameen M, Burden AD, Tillman D, Barker JN, Trembath RC (2004) A synonymous SNP of the corneodesmosin gene leads to increased mRNA stability and demonstrates association with psoriasis across diverse ethnic groups. Hum Mol Genet 13:2361–2368. doi:10.1093/hmg/ddh273

    Article  CAS  PubMed  Google Scholar 

  • Charru M, Seynave I, Morneau F, Bontemps J-D (2010) Recent changes in forest productivity: an analysis of national forest inventory data for common beech (Fagus sylvatica L.) in north-eastern France. Forest Ecol Manag 260:864–874. doi:10.1016/j.foreco.2010.06.005

    Article  Google Scholar 

  • Chen J, Tsuda Y, Stocks M, Källman T, Xu N, Kärkkäinen K, Huotari T, Semerikov VL, Vendramin GG, Lascoux M (2014) Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 and Gigantea? Genetics 197:1025–1038. doi:10.1534/genetics.114.163063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539. doi:10.1186/1471-2105-9-539

    Article  PubMed Central  PubMed  Google Scholar 

  • Derory J, Léger P, Garcia V, Schaeffer J, Hauser M-T, Salin F, Luschnig C, Plomion C, Glössl J, Kremer A (2006) Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol 170:723–738. doi:10.1111/j.1469-8137.2006.01721.x

    Article  CAS  PubMed  Google Scholar 

  • Durand J, Bodenes C, Chancerel E, Frigerio J-M, Vendramin G, Sebastiani F, Buonamici A, Gailing O, Koelewijn H-P, Villani F, Mattioni C, Cherubini M, Goicoechea PG, Herran A, Ikaran Z, Cabane C, Saneyoshi U, Alberto F, Dumoulin P-Y, Guichoux E, de Daruvar A, Kremer A, Plomion C (2010) A fast and cost-effective approach to develop and map EST-SSR markers: oak as a case study. BMC Genomics 11:570. doi:10.1186/1471-2164-11-570

    Article  PubMed Central  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, St. Clair JB, Neale DB (2009) Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold hardiness related traits. Genetics 182:1289–1302. doi:10.1534/genetics.109.102350

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eckert AJ, Jv H, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neale DB (2010) Patterns of population structure and environmental associations to aridity across the range of Loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982. doi:10.1534/genetics.110.115543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • European Environment Agency (EEA) (2012) Climate change, impact and vulnerability in Europe 2012, an indicator-based report. European Environment Agency, Copenhagen. doi:10.2800/66071

  • 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  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed Central  CAS  Google Scholar 

  • Foll M, Gaggiotti H (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993. doi:10.1534/genetics.108.092221

    Article  PubMed Central  PubMed  Google Scholar 

  • Gömöry D, Paule L (2011) Trade-off between height growth and spring flushing in common beech (Fagus sylvatica L). Ann For Sci 68:975–984. doi:10.1007/s13595-011-0103-1

    Article  Google Scholar 

  • González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409. doi:10.1534/genetics.106.061127

    Article  PubMed Central  PubMed  Google Scholar 

  • Hanewinkel M, Cullmann DA, Schelhaas M-J, Nabuurs G-J, Zimmermann NE (2013) Climate change may cause severe loss in the economic value of European forest land. Nature Clim Change 3:203–207. doi:10.1038/NCLIMATE1687

    Article  Google Scholar 

  • Henry P, Russello MA (2013) Adaptive divergence along environmental gradients in a climate-change-sensitive mammal. Ecol Evol 3:3906–3917. doi:10.1002/ece3.776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hertel D, Strecker T, Müller-Haubold H, Leuschner C (2013) Fine root biomass and dynamics in beech forests across a precipitation gradient—is optimal resource partitioning theory applicable to water-limited mature trees? J Ecol 101:1183–1200

    Article  Google Scholar 

  • Huang K, Whitlock R, Press MC, Scholes JD (2012) Variation for host range within and among populations of the parasitic plant Striga hermonthica. Heredity 108:96–104. doi:10.1038/hdy.2011.52

    Article  PubMed Central  CAS  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. doi:10.1534/genetics.107.082354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jochner S, Höfler J, Beck I, Göttlein A, Ankerst DP, Traidl-Hoffmann C, Menzel A (2013) Nutrient status: a missing factor in phenological and pollen research? J Exp Bot 64:2081–2092. doi:10.1093/jxb/ert061

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jump AS, Hunt JM, Martínez-Izquierdo JA, Peñuelas J (2006) Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol Ecol 15:3469–3480. doi:10.1111/j.1365-294X.2006.03027.x

    Article  CAS  PubMed  Google Scholar 

  • Kölling C, Walentowski H, Borchert H (2005) Die Buche in Mitteleuropa, eine Waldbaumart mit grandioser Vergangenheit und sicherer Zukunft. AFZ - Der Wald 13:696–701

    Google Scholar 

  • Körner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462. doi:10.1126/science.1186473

    Article  PubMed  Google Scholar 

  • Kraj W, Sztorc A (2009) Genetic structure and variability of phenological forms in the European beech (Fagus sylvatica L.). Ann For Sci 66:203. doi:10.1051/forest/2008085

    Article  Google Scholar 

  • Kreyling J, Thiel D, Nagy L, Jentsch A, Huber G, Konnert M, Beierkuhnlein C (2012) Late frost sensitivity of juvenile Fagus sylvatica L. differs between southern Germany and Bulgaria and depends on preceding air temperature. Eur J For Res 131:717–725. doi:10.1007/s10342-011-0544-y

    Article  Google Scholar 

  • Lalagüe H, Csilléry K, Oddou-Muratorio S, Safrana J, de Quattro C, Fady B, González-Martínez SC, Vendramin GG (2014) Nucleotide diversity and linkage disequilibrium at 58 stress response and phenology candidate genes in a European beech (Fagus sylvatica L.) population from southeastern France. Tree Genet Genomes 10:15–26. doi:10.1007/s11295-013-0658-0

    Article  Google Scholar 

  • Liesebach M (2012) Wachstum und Phänotypische Variation von sechs Herkünften der Rot-Buche (Fagus sylvatica L.) an einem Standort in Schleswig-Holstein. Appl Agric Forestry Res 62:179–192

    Google Scholar 

  • Long AD, Langley CH (1999) The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res 9:720–731. doi:10.1101/gr.9.8.720

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lüpke B (2004) Risikominderung durch Mischwälder und naturnaher Waldbau: ein Spannungsfeld. Forstarchiv 75:43–50

    Google Scholar 

  • Meier ES, Edwards TC Jr, Kienast F, Dobbertin M, Zimmermann NE (2011) Co-occurrence patterns of trees along macro-climatic gradients and their potential influence on the present and future distribution of Fagus sylvatica L. J Biogeogr 38:371–382. doi:10.1111/j.1365-2699.2010.02405.x

    Article  Google Scholar 

  • Müller M, Seifert S, Finkeldey R (2015) Identification of SNPs in candidate genes potentially involved in bud burst in European beech (Fagus sylvatica L.). Silvae Genet (in press)

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122. doi:10.1038/nrg2931

    Article  CAS  PubMed  Google Scholar 

  • Pastorelli R, Schmulders MJM, Van’t Westende WPC, Vosman B, Giannini R, Vettori C, Vendramin GG (2003) Characterization of microsatellite markers in Fagus sylvatica L. and Fagus orientalis Lipsky. Mol Ecol Notes 3:76–78. doi:10.1046/j.1471-8286.2003.00355.x

    Article  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peñuelas J, Boada M (2003) A global change-induced biome shift in Montseny mountains (NE Spain). Glob Change Biol 9:131–140. doi:10.1046/j.1365-2486.2003.00566.x

    Article  Google Scholar 

  • Pluess AR, Weber P (2012) Drought-adaptation potential in Fagus sylvatica: linking moisture availability with genetic diversity and dendrochronology. Plos One 7, e33636. doi:10.1371/journal.pone.0033636

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Prunier J, Pelgas B, Gagnon F, Desponts M, Isabel N, Beaulieu J, Bousquet J (2013) The genomic architecture and association genetics of adaptive characters using a candidate SNP approach in boreal black spruce. BMC Genomics 14:368. doi:10.1186/1471-2164-14-368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rajendra KC, Seifert S, Prinz K, Gailing O, Finkeldey R (2014) Sublte human impacts on neutral genetic diversity and spatial patterns of genetic variation in European beech (Fagus sylvatica L.) Forest Ecol Manag 319:138–149. doi:10.1016/j.foreco.2014.003

  • Rennenberg H, Seiler W, Matyssek R, Gessler A, Kreuzwieser J (2004) Die Buche (Fagus sylvatica L.) – ein Waldbaum ohne Zukunft im südlichen Mitteleuropa? All Forst-u J-Ztg 175:210–224

    Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    Article  PubMed  Google Scholar 

  • Sambrook J, Fischer EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Seifert S (2012) Variation of candidate genes related to climate change in European beech (Fagus sylvatica L.). Dissertation, Georg-August-University Göttingen

  • Seifert S, Vornam B, Finkeldey R (2012) DNA sequence variation and development of SNP markers in beech (Fagus sylvatica L.). Eur J For Res 131:1761–1770. doi:10.1007/s10342-012-0630-9

    Article  CAS  Google Scholar 

  • 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 Central  PubMed  Google Scholar 

  • Ueno S, Le Provost G, Léger V, Klopp C, Noirot C, Frigerio J-M, Salin F, Salse J, Abrouk M, Murat F, Brendel O, Derory J, Abadie P, Léger P, Cabane C, Barré A, de Daruvar A, Couloux A, Wincker P, Reviron M-P, Kremer A, Plomion C (2010) Bioinformatic analysis of ESTs collected by Sanger and pyrosequencing methods for a keystone forest tree species: oak. BMC Genomics 11:650. doi:10.1186/1471-2164-11-650

    Article  PubMed Central  PubMed  Google Scholar 

  • Vidalis A, Curtu AL, Finkeldey R (2013) Novel SNP development and analysis at a NADP+-specific IDH enzyme gene in a four species mixed oak forest. Plant Biol 15:126–137. doi:10.1111/j.1438-8677.2012.00575.x

    Article  CAS  PubMed  Google Scholar 

  • Vitasse Y (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol 198:149–155. doi:10.1111/nph.12130

    Article  PubMed  Google Scholar 

  • Vitasse Y, Basler D (2013) What role for photoperiod in the bud burst phenology of European beech. Eur J Forest Res 132:1–8. doi:10.1007/s10342-012-0661-2

    Article  Google Scholar 

  • Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A (2009) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J Forest Res 39:1259–1269. doi:10.1111/j.1438-8677.2012.00575.x

    Article  Google Scholar 

  • Vornam B, Decarli N, Gailing O (2004) Spatial distribution of genetic variation in a natural beech stand (Fagus sylvatica L.) based on microsatellite markers. Conserv Genet 5:561–570. doi:10.1023/B:COGE.0000041025.82917.ac

    Article  CAS  Google Scholar 

  • Wielgolaski FE (2001) Phenological modifications in plants by various edaphic factors. Int J Biometeorol 45:196–202. doi:10.1007/s004840100100

    Article  CAS  PubMed  Google Scholar 

  • Wühlisch Gv, Duval H, Jacques D, Muhs H-J (1995) Stability of differences in flushing between beech provenances in different years and at different sites. In: Madsen SF (ed.) Genetics and silviculture of beech: proceedings from the 5th beech symposium of the IUFRO project group P1.10-00, 19.-24. September 1994, Morgenstrup, Denmark. Danish Forest and Landscape Research Institute, Hørsholm, pp 83–89

  • Zhan X, Dixon A, Batbayar N, Bragin E, Ayas Z, Deutschova L, Chavko J, Domashevsky S, Dorosencu A, Bagyura J, Gombobaatar S, Grlica ID, Levin A, Milobog Y, Ming M, Prommer M, Purev-Ochir G, Ragyov D, Tsurkanu V, Vetrov V, Zubkov N, Bruford MW (2015) Exonic versus intronic SNPs: contrasting roles in revealing the population genetic differentiation of a widespread bird species. Heredity 114:1–9. doi:10.1038/hdy.2014.59

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by the Ministry for Science and Culture of Lower Saxony within the network KLIFF—climate impact and adaptation research in Lower Saxony. We thank A. Dolynska, C. Radler, G. Dinkel, and A. Capelle for their technical assistance as well as all persons who helped us with the field work.

Author information

Authors and Affiliations

  1. Forest Genetics and Forest Tree Breeding, Büsgen Institute, Faculty for Forest Sciences and Forest Ecology, Georg-August University Göttingen, Büsgenweg 2, 37077, Göttingen, Germany

    Markus Müller, Sarah Seifert & Reiner Finkeldey

Authors
  1. Markus Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Seifert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Reiner Finkeldey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Müller.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Data archiving statement

Genotype (SNP) data and phenotypic data were submitted to the TreeGenes Database (http://dendrome.ucdavis.edu/treegenes/; accession number TGDR040).

Additional information

Communicated by A. Kremer

This article is part of the Topical Collection on Complex Traits

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 65 kb)

ESM 2

(PDF 263 kb)

ESM 3

(PDF 260 kb)

ESM 4

(PDF 286 kb)

ESM 5

(PDF 371 kb)

ESM 6

(PDF 263 kb)

ESM 7

(PDF 1318 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Müller, M., Seifert, S. & Finkeldey, R. A candidate gene-based association study reveals SNPs significantly associated with bud burst in European beech (Fagus sylvatica L.). Tree Genetics & Genomes 11, 116 (2015). https://doi.org/10.1007/s11295-015-0943-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0943-1

Keywords

Search

Navigation