Abstract
Marker–trait associations based on populations from controlled crosses have been established in peach using markers mapped on the peach consensus map. In this study, we explored the utility of unstructured populations for association mapping to determine useful marker–trait associations in peach/nectarine cultivars. We used 94 peach cultivars representing local Spanish and modern cultivars from international breeding programs that are maintained at the Experimental Station of Aula Dei, Spain. This collection was characterized for pomological traits and was screened with 40 SSR markers that span the peach genome. Population structure analysis using STRUCTURE software identified two subpopulations, the local and modern cultivars, with admixture within both groups. The local Spanish cultivars were somewhat less diverse than modern cultivars. Marker–trait associations were determined in TASSEL with and without modelling coefficient of membership (Q) values as covariates. The results showed significant associations with pomological traits. We chose three markers on LG4 because of their proximity to the endoPG locus (freestone–melting flesh) that strongly affects pomological traits. Two genotypes of BPPCT015 marker showed significant associations with harvest date, flavonoids and sorbitol. Also, two genotypes of CPPCT028 showed associations with harvest date, total phenolics, RAC, and total sugars. Finally, two genotypes of endoPG1 showed associations with flesh firmness and total sugars. The analysis of linkage disequilibrium (LD) revealed a high level of LD up to 20 cM, and decay at farther distances. Therefore, association mapping could be a powerful tool for identifying marker–trait associations and would be useful for marker-assisted selection in peach breeding.
Similar content being viewed by others
References
Abidi W, Jiménez S, Moreno MA, Gogorcena Y (2011) Evaluation of antioxidant compounds and total sugar content in a nectarine [Prunus persica (L.) Batsch] progeny. Int J Mol Sci 12:6919–6935
Aranzana MJ, García-Mas J, Carbó J, Arús P (2002) Development and variability analysis of microsatellites markers in peach. Plant Breed 121:87–92
Aranzana MJ, Carbó J, Arús P (2003) Microsatellite variability in peach [Prunus persica (L.) Batsch]: cultivar identification, marker mutation, pedigree inferences and population structure. Theor Appl Genet 106:1341–352
Aranzana MJ, Abbassi EK, Howad W, Arús P (2010) Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet 11:69
Arús P, Verde I, Sosinski B, Zhebentyayeva TN, Abbott AB (2012) The peach genome. Tree Genet Genom 8:531–547
Badenes M, Werner DJ, Martínez-Calvo J, Lorente M, Llácer G (1998) An overview of the peach industry of Spain. Fruit Var J 52:11–17
Bassam BJ, Caetano-Anoelles G, Gresshoff PM (1983) Fast and sensitive silver staining of DNA in polyacrylamide gels. Ann Biochem 196:80–83
Bielenberg D, Gasic K, Chaparro JX (2009) An introduction to peach (Prunus persica). In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomics: crops and models 6. Springer, Heidelberg, pp 223–234
Bouhadida M, Casas AM, Moreno MA, Gogorcena Y (2007) Molecular characterization of Miraflores peach variety and relatives using SSRs. Sci Hortic 111:140–145
Bouhadida M, Casas AM, Gonzalo MJ, Arús P, Moreno MA, Gogorcena Y (2009) Molecular characterization and genetic diversity of Prunus rootstocks. Sci Hortic 120:237–245
Bouhadida M, Moreno MA, Gonzalo MJ, Alonso JM, Gogorcena Y (2011) Genetic variability of introduced and local Spanish peach cultivars determined by SSR markers. Tree Genet Genom 7:257–270
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free-radical method to evaluate antioxidant activity. Food Sci and Technol-Lebensm-Wissenschaft Technol 28:25–30
Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455
Bus V, Esmenjaud D, Buck E, Laurens F (2009) Application of genetic markers in Rosaceous crops. In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomics: crops and models 6. Springer, Heidelberg, pp 563–599
Cambra R (1988) Peaches in Spain. In: Childers NF, Sherman WB (eds) The peach. University of Florida, Gainesville, pp 186–189
Cantín CM, Gogorcena Y, Moreno MA (2009a) Analysis of phenotypic variation of sugar profile in different peach and nectarine [Prunus persica (L.) Batsch] breeding progenies. J Sci Food Agric 89:1909–1917
Cantín CM, Moreno MA, Gogorcena Y (2009b) Evaluation of the antioxidant capacity, phenolic compounds, and vitamin C content of different peach and nectarine [Prunus persica (L.) Batsch] breeding progenies. J Agric Food Chem 57:4586–4592
Cantín CM, Crisosto CH, Ogundiwin EA, Gradziel T, Torrents J, Moreno MA, Gogorcena Y (2010a) Chilling injury susceptibility in an intra-specific peach [Prunus persica (L.) Batsch] progeny. Post Biol Technol 58:79–87
Cantín CM, Gogorcena Y, Moreno MA (2010b) Phenotypic diversity and relationships of fruit quality traits in peach and nectarine [Prunus persica (L.) Batsch] breeding progenies. Euphytica 171:211–226
Cevallos-Casals BA, Byrne D, Okie WR, Cisneros-Zevallos L (2006) Selecting new peach and plum genotypes rich in phenolic compounds and enhanced functional properties. Food Chem 96:273–280
Cevik V, Ryder CD, Popovich A, Manning K, King GJ, Seymour GB (2010) A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh). Tree Genet Genom 6:271–279
Cipriani G, Lot G, Huang HG, Marrazzo MT, Peterlunger E, Testolin R (1999) AC/GT and AG/CT microsatellite repeats in peach [Prunus persica (L.) Batsch]: isolation, characterization and cross-species amplification in Prunus. Theor Appl Genet 99:65–72
Dirlewanger E, Arús P (2004) Markers in tree breeding: improvement of peach. Molecular marker systems in plant breeding and crop improvement. In: Lorz H, Wenzel G (eds) Biotechnology in agriculture and forestry, vol 55. Springer, Berlin, pp 279–302
Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A, Plomion C, Monet C (1999) Mapping QTLs controlling fruit quality in peach. Theor Appl Genet 98:18–31
Dirlewanger E, Cosson P, Travaud M, Aranzana MJ, Poizat C, Zanetto A, Arús P, Laigret F (2002) Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet 105:127–138
Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 29:9891–9896
Dirlewanger E, Cosson P, Boudehri K, Renaud C, Capdeville G, Tauzin Y, Laigret F, Moing A (2006) Development of a second-generation genetic linkage map for peach [Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genom 3:1–13
Downey LD, Iezzoni AF (2000) Polymorphic DNA markers in cherry are identified using sequences from sweet cherry, peach and sour cherry. J Am Soc Hortic Sci 125:76–80
Eduardo I, Pacheco I, Chietera G, Bassi D, Pozzi C, Vecchietti A, Rossini L (2011) QTL analysis of fruit quality traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genom 7:323–335
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
Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol 185:917–930
FAOSTAT (2012) http://faostat.fao.org
Flint-Garcia SA, Thornsberry JM, Buckler IV ES (2003) Structure of linkage disequilibrium in plants. Ann Rev Plant Biol 54:357–374
Font i Forcada C, Gogorcena Y, Moreno MA (2012) Agronomical and fruit quality traits of two peach cultivars on peach-almond hybrid rootstocks growing on Mediterranean conditions. Sci Hortic 140:157–163
Fuleki T, Francis FJ (1968) Quantitative methods for anthocyanins. 1. Extraction and determination of total anthocyanin in cranberries. J Food Sci 33:78–83
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
Gil MI, Tomás-Barberán FA, Hess-Pierce B, Kader AA (2002) Antioxidant capacities, phenolic compounds, carotenoids, and vitamin C contents of nectarine, peach, and plum cultivars from California. J Agric Food Chem 50:4976–4982
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glemin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24:1506–1517
Hedrick UP (1917) The peaches of New York. Report of the N.Y. Agricultural Experiment Station for the Year 1916. N.Y. Agricultural Experiment Station, Geneva
Herrero J (1953) Tree fruit growing in Spain. In: Fruit year book 1953. Royal Horticultural Society, London, pp. 50–63
Illa E, Eduardo I, Audergon JM, Barale F, Dirlewanger E, Li X, Moing A, Lambert P, Le Dantec L, Gao Z, Poëssel JL, Pozzi C, Rossini L, Vecchietti A, Arús P, Howad W (2011) Saturating the Prunus (stone fruits) genome with candidate genes for fruit quality. Mol Breed 28:667–682
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kloosterman AD, Budowle B, Daselaar P (1993) PCR-amplification and detection of the human DIS80 VNTR locus. Amplification conditions, population genetics and application in forensic analysis. Int J Leg Med 105:257–264
Le Dantec L, Cardinet G, Bonet J, Fouché M, Boudehri K, Monfort A, Poëssel JL, Moing A, Dirlewanger E (2010) Development and mapping of peach candidate genes involved in fruit quality and their transferability and potential use in other Rosaceae species. Tree Genet Genom 6:995–1012
Ledbetter C, Peterson S, Jenner J (2006) Modification of sugar profiles in California adapted apricots (Prunus armeniaca L.) through breeding with Central Asian germplasm. Euphytica 148:251–259
Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–398
Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63
Mariette S, Tavaud M, Arunyawat U, Capdeville G, Millan M, Salin F (2010) Population structure and genetic bottleneck in sweet cherry estimated with SSRs and the gametophytic self-incompatibility locus. BMC Genet 11:77
McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186:318–332
Mnejja M, García-Mas M, Howad W, Badenes ML, Arús P (2004) Simple sequence repeat (SSR) markers of Japanese plum (Prunus salicina Lindl.) are highly polymorphic and transferable to peach and almond. Mol Ecol Notes 4:163–166
Mnejja M, García-Mas M, Howad W, Arús P (2005) Development and transportability across Prunus species of 42 polymorphic almond microsatellites. Mol Ecol Notes 5:531–535
Monet R, Guye A, Roy M, Dachary N (1996) Peach mendelian genetics: a short review of results. Agronomie 16:321–329
Moreau L, Lemarie S, Charcosset A, Gallais A (2000) Economic efficiency of one cycle of marker-assisted selection. Crop Sci 40:329–337
Mounzer OH, Conejero W, Nicolás E, Abrisqueta I, García-Orellana YV, Tapia LM, Vera J, Abrisqueta JM, Ruiz-Sánchez MC (2008) Growth pattern and phenological 1128 stages of early-maturing peach trees under a Mediterranean climate. HortSci 43:1813–1818
Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang ZW, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Ogundiwin EA, Peace CP, Gradziel TM, Parfitt DE, Bliss FA, Crisosto CH (2009) A fruit quality gene map of Prunus. BMC Genom 10:587
Okie WR (1998) Handbook of peach and nectarine varieties: performance in the Southeastern United States and index of names. USDA Agriculture Handbook No. 714. US Department of Agriculture, Washington, DC
Oraguzie NC, Wilcox PL, Rikkerink EHA, De Silva HN (2007) Linkage disequilibrium. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, De Silva HN (eds) Association mapping in plants. Springer, New York, pp 11–39
Oraguzie NC, Whitworth CJ, Brewer L, Hall A, Volz RK, Bassett H, Gardiner SE (2010) Relationships of PpACS1 and PpACS2 genotypes, internal ethylene concentration and fruit softening in European (Pyrus communis) and Japanese (Pyrus pyrifolia) pears during cold air storage. Plant Breed 129:219–226
Peace CP, Crisosto CH, Gradziel TM (2005) Endopolygalacturonase: a candidate gene for freestone and melting flesh in peach. Mol Breed 16:21–31
Pozzi C, Vecchietti A (2009) Peach structural genomics. In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae, plant genetics and genomics: crops and models 6. Springer, Heidelberg, pp 235–257
Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181
Rohlf FJ (2000) NTSYS-pc Numerical taxonomy and multivariate analysis system, version 2.1. Exeter Software, Setauket
Sánchez-Pérez R, Howad D, Dicenta F, Arús P, Martínez-Gómez P (2007) Mapping major genes and quantitative trait loci controlling agronomic traits in almond. Plant Breed 126:310–318
Schulze TG, McMahon FJ (2002) Genetic association mapping at the crossroads: which test and why? Overview and practical guidelines. Am J Med Genet 114:1–11
Sharbel TF, Haubold B, Mitchell-Olds T (2000) Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol Ecol 9:2109–18
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Sosinski B, Gannavarapu M, Hager LD, Beck LE, King GJ, Ryder CD, Rajapakse S, Baird WV, Ballard RE, Abbott AG (2000) Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 101:421–428
Tavarini S, Degl’Innocenti E, Remorini D, Massai R, Guidi L (2008) Preliminary characterisation of peach cultivars for their antioxidant capacity. Int J Food Sci Technol 43:810–815
Testolin R, Marrazzo T, Cipriani G, Quarta R, Verde I, Dettori T, Pancaldi M, Sansavini S (2000) Microsatellite DNA in peach [Prunus persica (L.) Batsch] and its use in fingerprinting and testing the genetic origin of cultivars. Genome 43:512–520
Tomás-Barberán FA, Gil MI, Cremin P, Waterhouse AL, Hess-Pierce B, Kader AA (2001) HPLC-DAD-ESIMS analysis of phenolic compounds in nectarines, peaches and plums. J Agric Food Chem 49:4748–4760
Wilson LM, Whitt SR, Ibañez AM, Rocheford TR, Goodman MM, Buckler IV ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733
Yeh FC, Yang RC, Boyle T (1997) POPGENE. CIFOR and University of Alberta, Canada Version 1.21
Yousef GG, Juvik JA (2001) Comparison of phenotypic and marker-assisted selection for quantitative traits in sweet corn. Crop Sci 41:645–655
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotech 17:155–160
Zaharieva TB, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221:269–275
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559
Acknowledgments
We thank Blessing Athanson (Washington State University-IAREC USA), Rosa Giménez, Elvira Sierra, and Silvia Segura for technical assistance and plant management in the field. We gratefully acknowledge Dr. Chuck Brown (USDA-ARS, Prosser) for allowing us to use his ABI machine for fragment analyses and Dr. Ana Casas for assistance and support on the statistical analysis. This study was funded by the Spanish MICINN (Ministry of Science and Innovation) grants AGL-2008-00283 and RFP 2009-00016 and co-funded by FEDER and the Regional Government of Aragón (A44). C. Font was supported by a JAE-Pre fellowship from CSIC (Consejo Superior de Investigaciones Científicas) which enabled her to visit Washington State University, USA, to undertake a preliminary study of association genetics.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Abbott
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 4381 kb)
Rights and permissions
About this article
Cite this article
Font i Forcada, C., Oraguzie, N., Igartua, E. et al. Population structure and marker–trait associations for pomological traits in peach and nectarine cultivars. Tree Genetics & Genomes 9, 331–349 (2013). https://doi.org/10.1007/s11295-012-0553-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-012-0553-0