Skip to main content
Log in

Association Mapping in Turkish Olive Cultivars Revealed Significant Markers Related to Some Important Agronomic Traits

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Olive (Olea europaea L.) is one of the most important fruit trees especially in the Mediterranean countries due to high consumption of table olive and olive oil. In olive breeding, the phenotypic traits associated to fruit are the key factors that determine productivity. Association mapping has been used in some tree species and a lot of crop plant species, and here, we perform an initial effort to detect marker-trait associations in olive tree. In the current study, a total of 96 olive genotypes, including both oil and table olive genotypes from Turkish Olive GenBank Resources, were used to examine marker-trait associations. For olive genotyping, SNP, AFLP, and SSR marker data were selected from previously published study and association analysis was performed between these markers and 5 yield-related traits. Three different approaches were used to check for false-positive results in association tests, and association results obtained from these models were compared. Using the model utilizing both population structure and relative kinship, eleven associations were significant with FDR ≤ 0.05. The largest number of significant associations was detected for fruit weight and stone weight. Our results suggested that association mapping could be an effective approach for identifying marker-trait associations in olive genotypes, without the development of mapping populations. This study shows for the first time the use of association mapping for identifying molecular markers linked to important traits in olive tree.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aabidine AZE et al (2010) Construction of a genetic linkage map for the olive based on AFLP and SSR markers. Crop Sci 50:2291–2302

    Article  CAS  Google Scholar 

  • Abdurakhmonov IY, Abdukarimov A (2008) Application of association mapping to understanding the genetic diversity of plant germplasm resources. Int J Plant Genom. doi:10.1155/2008/574927

    Google Scholar 

  • Aranzana MJ, Abbassi E-K, Howad W, Arús P (2010) Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet 11:69

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arumugasundaram S, Ghosh M, Veerasamy S, Ramasamy Y (2011) Species discrimination, population structure and linkage disequilibrium in Eucalyptus camaldulensis and Eucalyptus tereticornis using SSR markers. PLoS One 6:e28252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atienza S, de la Rosa R, León L, Martín A, Belaj A (2014) Identification of QTL for agronomic traits of importance for olive breeding. Mol Breed 34:1–13

    Article  CAS  Google Scholar 

  • Baldoni L, Angiolillo A, Pellegrini M, Mencuccini M (1997) A linkage genome map for olive as an important tool for marker-assisted selection. In: Third international symposium on olive growing, vol. 474, pp 111–116

  • Barnaud A, Laucou V, This P, Lacombe T, Doligez A (2010) Linkage disequilibrium in wild French grapevine, Vitis vinifera L. subsp. silvestris. Heredity 104:431–437

    Article  CAS  PubMed  Google Scholar 

  • Belaj A, León L, Satovic Z, de la Rosa R (2011) Variability of wild olives (Olea europaea subsp. europaea var. sylvestris) analyzed by agro-morphological traits and SSR markers. Sci Hortic 129:561–569

    Article  Google Scholar 

  • Belaj A et al (2012) Developing a core collection of olive (Olea europaea L.) based on molecular markers (DArTs, SSRs, SNPs) and agronomic traits. Tree Genet Genomes 8:365–378

    Article  Google Scholar 

  • Bendini A, Cerretani L, Carrasco-Pancorbo A, Gómez-Caravaca AM, Segura-Carretero A, Fernández-Gutiérrez A, Lercker G (2007) Phenolic molecules in virgin olive oils: a survey of their sensory properties, health effects, antioxidant activity and analytical methods. An overview of the last decade. Alessandra Mol 12:1679–1719

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57(1):289–300

    Google Scholar 

  • Besnard G, El Bakkali A, Francki M (2014) Sequence analysis of single-copy genes in two wild olive subspecies: nucleotide diversity and potential use for testing admixture. Genome 57:145–153

    Article  CAS  PubMed  Google Scholar 

  • Boskou D (2006) Characteristics of the olive tree and olive fruit. Olive Oil Chem Technol 53:13–19

    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

    Article  CAS  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006a) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46:1323–1330

    Article  Google Scholar 

  • Breseghello F, Sorrells ME (2006b) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed  PubMed Central  Google Scholar 

  • Cantini C, Cimato A, Sani G (1999) Morphological evaluation of olive germplasm present in Tuscany region. Euphytica 109:173–181

    Article  Google Scholar 

  • Cao K, Wang L, Zhu G, Fang W, Chen C, Luo J (2012) Genetic diversity, linkage disequilibrium, and association mapping analyses of peach (Prunus persica) landraces in China. Tree Genet Genomes 8:975–990

    Article  Google Scholar 

  • Chhatre VE, Byram TD, Neale DB, Wegrzyn JL, Krutovsky KV (2013) Genetic structure and association mapping of adaptive and selective traits in the east Texas loblolly pine (Pinus taeda L.) breeding populations. Tree Genet Genomes 9:1161–1178

    Article  Google Scholar 

  • Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B 363:557–572

    Article  CAS  Google Scholar 

  • Covas M-I (2008) Bioactive effects of olive oil phenolic compounds in humans: reduction of heart disease factors and oxidative damage. Inflammopharmacology 16:216–218

    Article  CAS  PubMed  Google Scholar 

  • Cubry P et al (2013) An initial assessment of linkage disequilibrium (LD) in coffee trees: LD patterns in groups of Coffea canephora Pierre using microsatellite analysis. BMC Genom 14:10

    Article  CAS  Google Scholar 

  • De la Rosa R et al (2003) A first linkage map of olive (Olea europaea L.) cultivars using RAPD, AFLP, RFLP and SSR markers. Theor Appl Genet 106:1273–1282

    Article  PubMed  Google Scholar 

  • Deschamps S, Llaca V, May GD (2012) Genotyping-by-sequencing in plants. Biology 1:460–483

    Article  PubMed  PubMed Central  Google Scholar 

  • Dhanapal AP, Crisosto CH (2013) Association genetics of chilling injury susceptibility in peach (Prunus persica (L.) Batsch) across multiple years 3. Biotech 3:481–490

    Google Scholar 

  • Díez CM, Trujillo I, Barrio E, Belaj A, Barranco D, Rallo L (2011) Centennial olive trees as a reservoir of genetic diversity. Ann Bot 108:797–807

    Article  PubMed  PubMed Central  Google Scholar 

  • Dominguez-Garcia MdC et al (2012) Development of DArT markers in olive (Olea europaea L.) and usefulness in variability studies and genome mapping. Sci Hortic 136:50–60

    Article  CAS  Google Scholar 

  • Eckert AJ et al (2009) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas fir (Pseudotsuga menziesii var. menziesii). Genetics 183:289–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehrenreich IM, Stafford PA, Purugganan MD (2007) The genetic architecture of shoot branching in Arabidopsis thaliana: a comparative assessment of candidate gene associations vs. quantitative trait locus mapping. Genetics 176:1223–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Bakkali A, Haouane H, Moukhli A, Costes E, Van Damme P, Khadari B (2013) Construction of core collections suitable for association mapping to optimize use of Mediterranean olive (Olea europaea L.) genetic resources. PLoS One 8:e61265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El SN, Karakaya S (2009) Olive tree (Olea europaea) leaves: potential beneficial effects on human health. Nutr Rev 67:632–638

    Article  PubMed  Google Scholar 

  • Emanuelli F et al (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP The Plant. Genome 4:250–255

    Google Scholar 

  • FAOSTAT (2014) The statistical database (FAOSTAT). FAO, Rome

    Google Scholar 

  • Ferrão LFV et al (2014) The effects of encoding data in diversity studies and the applicability of the weighting index approach for data analysis from different molecular markers. Plant Syst Evol 300:1649–1661

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Flint-Garcia SA et al (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064

    Article  CAS  PubMed  Google Scholar 

  • Furlotte NA, Eskin E (2015) Efficient multiple trait association and estimation of genetic correlation using the matrix-variate linear mixed-model. Genetics. doi:10.1534/genetics.114.171447

    PubMed  PubMed Central  Google Scholar 

  • Galeano CH et al (2012) Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC Genet 13:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganopoulos IV, Kazantzis K, Chatzicharisis I, Karayiannis I, Tsaftaris AS (2011) Genetic diversity, structure and fruit trait associations in Greek sweet cherry cultivars using microsatellite based (SSR/ISSR) and morpho-physiological markers. Euphytica 181:237–251

    Article  Google Scholar 

  • García-Villalba R, Larrosa M, Possemiers S, Tomás-Barberán F, Espín J (2013) Bioavailability of phenolics from an oleuropein-rich olive (Olea europaea) leaf extract and its acute effect on plasma antioxidant status: comparison between pre-and postmenopausal women. Eur J Nutr 53(4):1–13

    Google Scholar 

  • Garris AJ, McCOUCH SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759–769

    PubMed  PubMed Central  Google Scholar 

  • Gebhardt C, Valkonen JP (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102

    Article  CAS  PubMed  Google Scholar 

  • Ghanbari R, Anwar F, Alkharfy KM, Gilani A-H, Saari N (2012) Valuable nutrients and functional bioactives in different parts of olive (Olea europaea L.)—a review. Int J Mol Sci 13:3291–3340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green P (2002) A revision of Olea L. (Oleaceae). Kew Bull 57:91–140

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Hannachi H, Breton C, Msallem M, Ben El Hadj S, El Gazzah M, Bervillé A (2008) Differences between native and introduced olive cultivars as revealed by morphology of drupes, oil composition and SSR polymorphisms: a case study in Tunisia. Sci Hortic 116:280–290

    Article  CAS  Google Scholar 

  • Haouane H et al (2011) Genetic structure and core collection of the World Olive Germplasm Bank of Marrakech: towards the optimised management and use of Mediterranean olive genetic resources. Genetica 139:1083–1094

    Article  PubMed  PubMed Central  Google Scholar 

  • Hong EP, Park JW (2012) Sample size and statistical power calculation in genetic association studies. Genom Informatics 10:117–122

    Article  Google Scholar 

  • i Forcada CF, Oraguzie N, Reyes-Chin-Wo S, Espiau MT, i Martí AF (2015) Identification of genetic loci associated with quality traits in almond via association mapping. PloS One 10:e0127656

    Article  CAS  Google Scholar 

  • Ibtissem L, Mouna MA, Messaoud M (2014) Phenotypic diversity of some olive tree progenies issued from a Tunisian breeding program. Eur Sci J 10(6):292–313

    Google Scholar 

  • IOOC (2011) Methodology for the Characterization of Olive Varieties Madrid, Spain COI/OH/Doc. No 1

  • Ipek A, Barut E, Gulen H, Ipek M (2012) Assessment of inter-and intra-cultivar variations in olive using SSR markers. Scientia Agricola 69:327–335

    Article  CAS  Google Scholar 

  • Iqbal MJ et al (2012) Population structure and linkage disequilibrium in Lupinus albus L. germplasm and its implication for association mapping. Theor Appl Genet 125:517–530

    Article  CAS  PubMed  Google Scholar 

  • Isik N, Doğanlar S, Frary A (2011) Genetic diversity of Turkish olive varieties assessed by simple sequence repeat and sequence-related amplified polymorphism markers. Crop Sci 51:1646–1654

    Article  CAS  Google Scholar 

  • Jaiswal V, Mir R, Mohan A, Balyan H, Gupta P (2012) Association mapping for pre-harvest sprouting tolerance in common wheat (Triticum aestivum L.). Euphytica 188:89–102

    Article  CAS  Google Scholar 

  • Jannink J-L, Bink MC, Jansen RC (2001) Using complex plant pedigrees to map valuable genes. Trends Plant Sci 6:337–342

    Article  CAS  PubMed  Google Scholar 

  • Kadkhodaei S et al (2011) Molecular tagging of agronomic traits using simple sequence repeats: Informative markers for almond (‘Prunus dulcis’) molecular breeding. Aust J Crop Sci 5:1199

    CAS  Google Scholar 

  • Kaya HB, Cetin O, Kaya H, Sahin M, Sefer F, Kahraman A, Tanyolac B (2013) SNP discovery by Illumina-based transcriptome sequencing of the olive and the genetic characterization of Turkish olive genotypes revealed by AFLP, SSR and SNP markers. PloS One 8:e73674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khadari B et al (2010) A genetic linkage map of olive based on amplified fragment length polymorphism, intersimple sequence repeat and simple sequence repeat markers. J Am Soc Hortic Sci 135:548–555

    Google Scholar 

  • Khadivi-Khub A (2014) Regression association analysis of fruit traits with molecular markers in cherries. Plant Syst Evol 300:1163–1173

    Article  CAS  Google Scholar 

  • Khan MA, Korban SS (2012) Association mapping in forest trees and fruit crops. J Exp Bot 105:447–456

    Google Scholar 

  • Kosman E, Leonard K (2005) Similarity coefficients for molecular markers in studies of genetic relationships between individuals for haploid, diploid, and polyploid species. Mol Ecol 14:415–424

    Article  CAS  PubMed  Google Scholar 

  • Kraakman AT, Niks RE, Van den Berg PM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krill AM, Kirst M, Kochian LV, Buckler ES, Hoekenga OA (2010) Association and linkage analysis of aluminum tolerance genes in maize. PLoS One 5:e9958

    Article  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon S-J et al (2008) QTL mapping of agronomic traits using an RIL population derived from a cross between temperate japonica cultivars in rice (Oryza sativa L.). Breed Sci 58:271–279

    Article  Google Scholar 

  • Laidò G, Marone D, Russo MA, Colecchia SA, Mastrangelo AM, De Vita P, Papa R (2014) Linkage disequilibrium and genome-wide association mapping in tetraploid wheat (Triticum turgidum L.). PLoS One 9:e95211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Larsson SJ, Lipka AE, Buckler ES (2013) Lessons from dwarf8 on the strengths and weaknesses of structured association mapping. PLoS Genet 9:e1003246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavee S, Haskal A, Avidan B (2012) The effect of planting distances and tree shape on yield and harvest efficiency of cv. Manzanillo table olives. Sci Hortic 142:166–173

    Article  Google Scholar 

  • León L, Martín LM, Rallo L (2004) Phenotypic correlations among agronomic traits in olive progenies. J Am Soc Hortic Sci 129:271–276

    Google Scholar 

  • León L, Beltrán G, Aguilera MP, Rallo L, Barranco D, De la Rosa R (2011) Oil composition of advanced selections from an olive breeding program. Eur J Lipid Sci Technol 113:870–875

    Article  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 Genomes 8:113–126

    Article  Google Scholar 

  • Li Z, Mu P, Li C, Zhang H, Gao Y, Wang X (2005) QTL mapping of root traits in a doubled haploid population from a cross between upland and lowland japonica rice in three environments. Theor Appl Genet 110:1244–1252

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Haseneyer G, Schön C-C, Ankerst D, Korzun V, Wilde P, Bauer E (2011) High levels of nucleotide diversity and fast decline of linkage disequilibrium in rye (Secale cereale L.) genes involved in frost response. BMC Plant Biol 11:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Long Y, Zhang C, Meng J (2008) Challenges for QTL analysis in crops. Crop Sci Biotech 11:7–12

    Google Scholar 

  • Ma X, Ding Y, Zhou B, Guo W, Lv Y, Zhu X, Zhang T (2008) QTL mapping in A-genome diploid Asiatic cotton and their congruence analysis with AD-genome tetraploid cotton in genus Gossypium. J Genet Genomics 35:751–762

    Article  PubMed  Google Scholar 

  • McKay SJ (2010) The genetic dissection of fruit texture traits in the apple cultivar Honeycrisp. University of Minnesota, Minneapolis

    Google Scholar 

  • Montilla-Bascón G et al. (2015) Genome-wide association study for crown rust (Puccinia coronata f. sp. avenae) and powdery mildew (Blumeria graminis f. sp. avenae) resistance in an oat (Avena sativa) collection of commercial varieties and landraces. Front Plant Sci 6

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nimmakayala P et al (2014) Linkage disequilibrium and population-structure analysis among Capsicum annuum L. cultivars for use in association mapping. Molecular Genetics and Genomics 289:1–9

    Article  CAS  Google Scholar 

  • Olukolu B (2010) The genetics of chilling requirements in apricot (Prunus armeniaca L.). Dissertation, Clemson University

  • Pace J, Gardner C, Romay C, Ganapathsybrumanian B, Lübberstedt T (2015) Genome-wide association analysis of seedling root development in maize (Zea mays L.). BMC Genom 16:47

    Article  CAS  Google Scholar 

  • Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, Kilian B, Graner A (2012) Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Biol 12:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira JA et al (2006) Table olives from Portugal: phenolic compounds, antioxidant potential, and antimicrobial activity. J Agric Food Chem 54:8425–8431

    Article  CAS  PubMed  Google Scholar 

  • Pozniak C, Clarke J, Clarke F (2012) Potential for detection of marker–trait associations in durum wheat using unbalanced, historical phenotypic datasets. Mol Breed 30:1537–1550

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180

    Article  CAS  PubMed  Google Scholar 

  • Reale S et al (2006) SNP-based markers for discriminating olive (Olea europaea L.) cultivars. Genome 49:1193–1205

    Article  CAS  PubMed  Google Scholar 

  • Rikkerink EH, Oraguzie NC, Gardiner SE (2007) Prospects of association mapping in perennial horticultural crops. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, de Silva HN (eds) Association mapping in plants. Springer, New York, pp 249–269

    Chapter  Google Scholar 

  • Sadok IB et al (2013) QTL mapping of flowering and fruiting traits in olive. PLoS One 8:e62831

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saeed M, Wangzhen G, Tianzhen Z (2014) Association mapping for salinity tolerance in cotton (‘Gossypium hirsutum’ L.) germplasm from US and diverse regions of China

  • Sakiroglu M, Sherman-Broyles S, Story A, Moore KJ, Doyle JJ, Brummer EC (2012) Patterns of linkage disequilibrium and association mapping in diploid alfalfa (M. sativa L.). Theor Appl Genet 125:577–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semagn K, Bjørnstad Å, Xu Y (2010) The genetic dissection of quantitative traits in crops. Electron J Biotechnol 13:16–17

    Article  Google Scholar 

  • Semon M, Nielsen R, Jones MP, McCouch SR (2005) The population structure of African cultivated rice Oryza glaberrima (Steud.) evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation. Genetics 169:1639–1647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shulaev V et al (2008) Multiple models for Rosaceae genomics Plant physiology 147:985–1003

    CAS  PubMed  Google Scholar 

  • Simko I, Costanzo S, Haynes K, Christ B, Jones R (2004) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene approach. Theor Appl Genet 108:217–224

    Article  CAS  PubMed  Google Scholar 

  • Skøt L et al (2007) Association of candidate genes with flowering time and water-soluble carbohydrate content in Lolium perenne (L.). Genetics 177:535–547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Slatkin M (2008) Linkage disequilibrium—understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9:477–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soto-Cerda BJ, Duguid S, Booker H, Rowland G, Diederichsen A, Cloutier S (2014) Association mapping of seed quality traits using the Canadian flax (Linum usitatissimum L.) core collection. Theor Appl Genet 127:881–896

    Article  PubMed  PubMed Central  Google Scholar 

  • Szalma S, Buckler E IV, Snook M, McMullen M (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theoretical and Applied Genetics 110:1324–1333

    Article  CAS  PubMed  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  PubMed  Google Scholar 

  • Tripoli E, Giammanco M, Tabacchi G, Di Majo D, Giammanco S, La Guardia M (2005) The phenolic compounds of olive oil: structure, biological activity and beneficial effects on human health. Nutr Res Rev 18:98–112

    Article  CAS  PubMed  Google Scholar 

  • TUIK (2016) Turkish Statistical Institute

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using QQ and manhattan plots. bioRxiv. doi:10.1101/005165

    Google Scholar 

  • Uchiyama K et al (2013) Demonstration of genome-wide association studies for identifying markers for wood property and male strobili traits in Cryptomeria japonica. PloS One 8:e79866

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uylaser V, Yildiz G (2013) Fatty acid profile and mineral content of commercial table olives from Turkey. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 41:518–523

    CAS  Google Scholar 

  • Van Inghelandt D, Reif JC, Dhillon BS, Flament P, Melchinger AE (2011) Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor Appl Genet 123:11–20

    Article  PubMed  Google Scholar 

  • Varshney RK, Chabane K, Hendre PS, Aggarwal RK, Graner A (2007) Comparative assessment of EST-SSR, EST-SNP and AFLP markers for evaluation of genetic diversity and conservation of genetic resources using wild, cultivated and elite barleys. Plant Sci 173:638–649

    Article  CAS  Google Scholar 

  • Virk PS, Ford-Lloyd BV, Jackson MT, Pooni HS, Clemeno TP, Newbury HJ (1996) Predicting quantitative variation within rice germplasm using molecular markers. Heredity 76:296–304

    Article  Google Scholar 

  • Visioli F, Bellomo G, Montedoro G, Galli C (1995) Low density lipoprotein oxidation is inhibited in vitro by olive oil constituents. Atherosclerosis 117:25–32

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Collins G, Sedgley M (2004) A molecular linkage map of olive (Olea europaea L.) based on RAPD, microsatellite, and SCAR markers. Genome 47:26–35

    Article  CAS  PubMed  Google Scholar 

  • Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210

    Article  PubMed  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (L.) genetic improvement. Crop Sci 51:433–449

    Article  Google Scholar 

  • Yang X et al (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431

    Article  PubMed  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160

    Article  CAS  PubMed  Google Scholar 

  • Yu J et al (2005) 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 

  • Yu H, Deng Z, Xiang C, Tian J (2012) Analysis of diversity and linkage disequilibrium mapping of agronomic traits on B-genome of wheat. J Genom 1:78–88

    Google Scholar 

  • Zhang P, Liu X, Tong H, Lu Y, Li J (2014) Association mapping for important agronomic traits in core collection of rice (Oryza sativa L.) with SSR markers. PLoS One 9:e111508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao K et al (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Wang H, Chen W, Li Y (2014) Genetic structure, linkage disequilibrium and association mapping of verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS One 9:e86308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Jean-Luc Jannink from Cornell University, Ithaca, NY, USA for many helpful suggestions for improving of this article. Special thanks to Deniz Akdemir and Julio Sanchez, from Cornell University, Ithaca, NY, USA for their helpful discussions. We thank Tugba Keskin Gundogdu from Ege University, Turkey for assistance in phenotypic data evaluation. We are grateful to Gunter Backes from University of Kassel, Germany for kindly sharing his experience in AM.

Funding

This study was funded by Scientific and Technical Research Council of Turkey with the project number 108G096.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bahattin Tanyolac.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaya, H.B., Cetin, O., Kaya, H.S. et al. Association Mapping in Turkish Olive Cultivars Revealed Significant Markers Related to Some Important Agronomic Traits. Biochem Genet 54, 506–533 (2016). https://doi.org/10.1007/s10528-016-9738-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-016-9738-9

Keywords

Navigation