Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genetic mapping of EST-derived simple sequence repeats (EST-SSRs) to identify QTL for leaf morphological characters in a Quercus robur full-sib family

  • 658 Accesses

  • 11 Citations

Abstract

The availability of genomic resources such as expressed sequence tag-derived simple sequence repeat (EST-SSR) markers in adaptive genes with high transferability across related species allows the construction of genetic maps and the comparison of genome structure and quantitative trait loci (QTL) positions. In the present study, genetic linkage maps were constructed for both parents of a Quercus robur × Q. robur ssp. slavonica full-sib pedigree. A total of 182 markers (61 AFLPs, 23 nuclear SSRs, 98 EST-SSRs) and 172 markers (49 AFLPs, 21 nSSRs, 101 EST-SSRs, 1 isozyme) were mapped on the female and male linkage maps, respectively. The total map length and average marker spacing were 1,038 and 5.7 cM for the female map and 998.5 and 5.8 cM for the male map. A total of 68 nuclear SSRs and EST-SSRs segregating in both parents allowed to define homologous linkage groups (LG) between both parental maps. QTL for leaf morphological traits were mapped on all 12 LG at a chromosome-wide level and on 6 LG at a genome-wide level. The phenotypic effects explained by each single QTL ranged from 4.0 % for leaf area to 15.8 % for the number of intercalary veins. QTL clusters for leaf characters that discriminate between Q. robur and Quercus petraea were mapped reproducibly on three LG, and some putative candidate genes among potentially many others were identified on LG3 and LG5. Genetic linkage maps based on EST-SSRs can be valuable tools for the identification of genes involved in adaptive trait variation and for comparative mapping.

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

References

  1. Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238

  2. Aldrich P, Cavender-Bares J (2011) Quercus. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, forest trees. Springer, Berlin, pp 89–129

  3. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  4. Banyai W, Kirdmanee C, Mii M, Supaibulwatana K (2010) Overexpression of farnesyl pyrophosphate synthase (FPS) gene affected artemisinin content and growth of Artemisia annua L. Plant Cell Tissue Organ Cult 103:255–265

  5. Beavis WD (1998) QTL analysis: power, precision, and accuracy. In: Paterson AH (ed) Molecular dissection of complex traits. CRC, Boca Raton, pp 145–162

  6. Bergelson J, Roux F (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11:867–879

  7. Bodénès C, Chancerel E, Gailing O, Vendramin GG, Bagnoli F, Durand J, Goicoechea PG, Soliani C, Villani F, Mattioni C, Koelewijn HP, Murat F, Salse J, Roussel G, Boury C, Alberto F, Kremer A, Plomion C (2012) Comparative mapping in the Fagaceae and beyond with EST-SSRs. BMC Plant Biol 12:153

  8. Burke JM, Lai Z, Salmaso M, Nakazato T, Tang SX, Heesacker A, Knapp SJ, Rieseberg LH (2004) Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167:449–457

  9. Casasoli M, Derory J, Morera-Dutrey C, Brendel O, Porth I, Guehl JM, Villani F, Kremer A (2006) Comparison of quantitative trait loci for adaptive traits between oak and chestnut based on an expressed sequence tag consensus map. Genetics 172:533–546

  10. Chagne D, Brown G, Lalanne C, Madur D, Pot D, Neale D, Plomion C (2003) Comparative genome and QTL mapping between maritime and loblolly pines. Mol Breed 12:185–195

  11. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

  12. Dow BD, Ashley MV (1996) Microsatellite analysis of seed dispersal and parentage of saplings in bur oak, Quercus macrocarpa. Mol Ecol 5:615–627

  13. Durand J, Bodénès C, Chancerel E, Frigero J-M, Vendramin GG, Sebastiani F, Buonamici A, Gailing O, Koelewijn H-P, Villani F, Mattioni C, Cherubini M, Goicoechea PG, Herran A, Ikaran Z, Cabane C, Ueno S, 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

  14. Ellis JR, Burke JM (2007) EST-SSRs as a resource for population genetic analyses. Heredity 99:125–132

  15. Gailing O (2008) QTL analysis of leaf morphological characters in a Quercus robur full-sib family (Q. robur x Q. robur ssp slavonica). Plant Biol 10:624–634

  16. Gailing O, Langenfeld-Heyser R, Polle A, Finkeldey R (2008) Quantitative trait loci affecting stomatal density and growth in a Quercus robur progeny: implications for the adaptation to changing environments. Glob Chang Biol 14:1934–1946

  17. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross mapping strategy and RAPD markers. Genetics 137:1121–1137

  18. Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

  19. Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186

  20. Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Van Dam B, Ducousso A, Forrest I, Lopez de Heredia U, Lowe AJ, Tutkova M, Munro RC, Steinhoff S, Badeau V (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann For Sci 59:777–787

  21. Kremer A, Casasoli M, Barreneche T, Bodénès C, Sisco P, Kubisiak T, Scalfi M, Leonardi E, Bakker E, Buiteveldt J, Romero-Severson J, Arumuganathan K, Derory J, Scotti-Saintagne C, Roussel G, Bertocchi E, Lexer C, Porth I, Hebard F, Clark C, Carlson J, Plomion C, Koelewijn H-P, Villani F (2007) Fagaceae trees. In: Kole C (ed) Genome mapping and molecular breeding in plants, volume 7. Forest trees. Springer, Berlin, pp 161–187

  22. Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

  23. Lind J, Gailing O (2013) Genetic structure of Quercus rubra L. and Q. ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genet Genomes. doi:10.1007/s11295-012-0586-4

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

  25. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377

  26. Novaes E, Osorio L, Drost DR, Miles BL, Boaventura-Novaes CRD, Benedict C, Dervinis C, Yu Q, Sykes R, Davis M, Martin TA, Peter GF, Kirst M (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 182:878–890

  27. Saintagne C, Bodénès C, Barreneche T, Pot D, Plomion C, Kremer A (2004) Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 92:20–30

  28. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

  29. Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Burg K, Glössl J (1997) Identification and characterization of (GA/CT)n-microsatellite loci from Quercus petraea. Plant Mol Biol 33:1093–1096

  30. Sullivan A, Lind J, McCleary TS, Romero-Severson J, Gailing O (2013) Development and characterization of genomic and gene-based microsatellite markers in North American red oak species. Plant Mol Biol Report 31:231–239. doi:10.1007/s11105-012-0495-6

  31. Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–233

  32. Ueno S, Le Provost G, Leger V, Klopp C, Noirot C, Frigerio JM, Salin F, Salse J, Abrouk M, Murat F, Brendel O, Derory J, Abadie P, Leger P, Cabane C, Barre A, de Daruvar A, Couloux A, Wincker P, Reviron MP, Kremer A, Plomion C (2010) Bioinformatic analysis of ESTs collected by Sanger and pyrosequencing methods for a keystone forest tree species: oak. BMC Genomics 11:24

  33. Van Ooijen JW (2004) MapQTL 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma, Wageningen

  34. Van Ooijen JW (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma, Wageningen

  35. Varshney RK, Sigmund R, Borner A, Korzun V, Stein N, Sorrells ME, Langridge P, Graner A (2005) Interspecific transferability and comparative mapping of barley EST-SSR markers in wheat, rye and rice. Plant Sci 168:195–202

  36. Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14:2095–2106

  37. Yin TM, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463

Download references

Acknowledgments

The authors are grateful to Olga Artes, Oleksandra Dolynska, and Christine Radler for their technical support in the lab and Martha Fernandez for her help in measuring leaves. Part of the study was supported by the European Commission under the FP6 program (Network of Excellence EVOLTREE (No. 016322, Evolution of Trees as Drivers of Terrestrial Biodiversity, http://www.evoltree.eu).

Data Archiving Statement

Data used in this manuscript have been made publicly available through the Quercus Portal (https://w3.pierroton.inra.fr/QuercusPortal/index.php) and will be submitted to the TreeGenes Database.

Author information

Correspondence to Oliver Gailing.

Additional information

Communicated by S. González-Martínez

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(DOCX 13 kb)

Supplementary Table 2

(DOCX 16 kb)

Supplementary Table 3

(XLS 230 kb)

Supplementary Table 4

(XLS 62 kb)

Supplementary Fig. 1

Genetic linkage maps showing 12 male (LG1m to LG12m) and 12 female (LG1f to LG12f) linkage groups. Markers that are shared between male and female linkage groups are connected by lines. Markers showing significant segregation distortion in the male or female parent are indicated by asterisks. AFLP markers are named using the nomenclature by Keygene and indicating the size of the fragment (e.g. P13/M66_112, see Gailing et al. 2008). EST-SSR markers are named according to Durand et al. (2010) using identifiers for the labs in which the markers were developed (e.g. PIE, FIR, GOT, POR). Indices a, b, etc. are added to names (e.g. POR045b) when more than one gene locus was amplified. *: 0.1 level, **: 0.05 level, ***: 0.01 level, ****: 0.005 level, *****: 0.001 level, ******: 0.0005 level (PPTX 785 kb)

Supplementary Fig. 2

QTL for leaf traits on male and female linkage groups. Arrows indicate the positions of the maximum LOD score and vertical lines show the map intervals with LOD scores above the 5 % chromosome-wide significance threshold. Frames show QTL at genome-wide significance level (p < 0.05), other QTL were significant only at the chromosome level (p < 0.05). QTL identified in at least two years on the same linkage group considering both male and female maps are labeled in bold and red. Markers showing significant segregation distortion in the male or female parent are indicated by asterisks. *: 0.1 level, **: 0.05 level, ***: 0.01 level, ****: 0.005 level, *****: 0.001 level, ******: 0.0005 level (PPTX 717 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gailing, O., Bodénès, C., Finkeldey, R. et al. Genetic mapping of EST-derived simple sequence repeats (EST-SSRs) to identify QTL for leaf morphological characters in a Quercus robur full-sib family. Tree Genetics & Genomes 9, 1361–1367 (2013). https://doi.org/10.1007/s11295-013-0633-9

Download citation

Keywords

  • Oaks
  • Linkage maps
  • Adaptive traits
  • Comparative mapping