Mapping QTLs associated with fruit quality traits in peach Prunus persica (L.) Batsch using SNP maps

[EN] Fruit quality is an essential criterion used to select new cultivars in peach breeding programs and is determined based on a combination of organoleptic and nutritional traits. The aim of this study was to identify quantitative trait loci (QTLs) for fruit quality traits in an F-1 nectarine population derived from 'Venus' and 'Big Top' cultivars. The progeny were evaluated over 4 years for agronomical and biochemical characteristics and genotyped using simple sequence repeat (SSR) markers and 'IPSC 9K peach SNP array v1'. Two genetic maps were constructed using 411 markers. The 'Venus' map spanned 259 cM on nine linkage groups (LGs) with 104 markers. The 'Big Top' map spanned 464 cM on 10 LGs with 122 markers. Single or Multiple QTL models mapping was applied separately for each year and all years combined. A total of 54 QTLs mapped over 12 LGs belonged to seven peach chromosomes. Most of the QTLs were consistent over the 4 years of study and were validated with the multi-year analysis. QTLs for total phenolic, flavonoid, and anthocyanin contents were reported for the first time in peach. LG 4 in 'Venus' and LG 5 in 'Big Top' showed the highest numbers of QTLs. This work represents the first study in an F-1 nectarine family to identify peach genomic regions that control fruit quality traits using 'IPSC 9K SNP array v1' and provides useful information for marker-assisted breeding to produce peaches with better antioxidant content and healthy attributes.We are grateful to C.H. Crisosto (University of California, Davis) for providing SSR markers (UCDCH15 and BINEPPCU6377). We thank E. Sierra and S. Segura for the technical assistance and plant management in the field and N. Ksouri for the bioinformatic assistance. We are grateful to A. Casas and E. Igartua for the assistance and support with the statistical analysis using JoinMap (R) 4 software. This study was funded by the Spanish Ministry of Economy and Competitiveness (MINECO) grants AGL-2008-00283, AGL2011-24576, and AGL2014-52063-R and was co-funded by the FEDER and the Regional Government of Aragon (A44) with European Social Fund. W. Abidi was supported by a JAE-Pre fellowship from the Consejo Superior de Investigaciones Cientificas (CSIC), which enabled him to visit the University of California, Davis, and the IBMCP, Valencia, Spain. J.L. Zeballos received a master fellow funded by the Spanish Agency for International Cooperation and Development (AECID).Zeballos, JL.; Adibi, W.; Giménez Millán, R.; Monforte Gilabert, AJ.; Moreno, MA.; Gogorcena, Y. (2016). Mapping QTLs associated with fruit quality traits in peach Prunus persica (L.) Batsch using SNP maps. Tree Genetics and Genomes. 12(3):1-17. https://doi.org/10.1007/s11295-016-0996-9S117123Abbott AG, Rajapakse S, Sosinski B, Lu ZX, Sossey-Alaoui K, Gannavarapu M, Reighard G, Ballard RE, Baird WV, Scorza R, Callahan A (1998) Construction of saturated linkage maps of peach crosses segregating for characters controlling fruit quality, tree architecture and pest resistance. Acta Hortic 465:41–50Abidi W, Jiménez S, Moreno MÁ, Gogorcena Y (2011) Evaluation of antioxidant compounds and total sugar content in a nectarine [Prunus persica (L.) Batsch] progeny. Int J Mol Sci 12:6919–6935Abidi W, Cantín C, Gonzalo MJ, Moreno MA, Gogorcena Y (2012) Genetic control and location of QTLs involved in antioxidant capacity and fruit quality traits in peach [Prunus persica (L.) Batch]. Acta Hortic 962:129–134Abidi W, Cantín CM, Jiménez S, Giménez R, Moreno MA, Gogorcena Y (2015) Effect of antioxidant compounds and total sugars and genetic background on the chilling injury susceptibility of a non-melting peach [Prunus persica (L.) Batsch] progeny. J Sci Food Agric 95:351–358Albrechtsen A, Nielsen FC, Nielsen R (2010) Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 11:2534–2547Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG (2012) The peach genome. Tree Genet Genomes 8:531–547Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A, Leschik-Bonnet E, Müller MJ et al (2012) Critical review: vegetables and fruit in the prevention of chronic diseases. Eur J Nutr 51:637–663Brem RB, Kruglyak L (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci U S A 102:1572–1577Broman KW, Saunak S (2009) A guide to QTL mapping with R/qtl. Statistic for biology and health. Springer, New York. doi: 10.1007/978-0-387-92125-9Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890Byrne DH, Raseira MB, Bassi D, Piagnani MC, Gasic K, Moreno MA, Pérez S (2012) Peach. In: Badenes ML, Byrne DH (eds) Fruit breeding, vol 8. Handbook of plant breeding, vol 8. Springer, New York, pp 505–569Cantín 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 89:1909–1917Cantín 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 57:4586–4592Cantín 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. Postharvest Biol Technol 58:79–87Cantín 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 171:211–226Crisosto CH (2002) How do we increase peach consumption? Acta Hortic 592:601–605Chagné D, Krieger C, Rassam M, Sullivan M, Fraser J, André C, Pindo M, Troggio M, Gardiner SE, Henry RA, Allan AC, McGhie TK, Laing WA (2012) QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol 12:1–16Chaparro JX, Werner DJ, O’Malley D, Sederoff RR (1994) Targeted mapping and linkage analysis of morphological isozyme, and RAPD markers in peach. Theor Appl Genet 87:805–815Da Silva Linge C, Bassi D, Bianco L, Pacheco I, Pirona R, Rossini L (2015) Genetic dissection of fruit weight and size in an F2 peach (Prunus persica (L.) Batsch) progeny. Mol Breed 35:71Davey MW, Kenis K, Keulemans J (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142:343–351Dirlewanger E, Pronier V, Parvery C, Rothan C, Guye A, Monet R (1998) Genetic linkage map of peach [Prunus persica (L.) Batsch] using morphological and molecular markers. Theor Appl Genet 97:888–895Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A, Plomion C, Monet R (1999) Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet 98(1):18–31Dirlewanger E, Graziano E, Joobeur T, Garriga-Calderé F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci U S A 101:9891–9896Dirlewanger E, Cosson P, Renaud C, Monet R, Poëssel JL, Moing A (2006) New detection of QTLs controlling major fruit quality components in peach. Acta Hortic 713:65–72Dirlewanger E, Quero-García J, Le Dantec L, Lambert P, Ruiz D, Dondini L, Illa E, Quilot-Turion B, Audergon JM, Tartarini S, Letourmy P, Arús P (2012) Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity 109:280–292Eduardo 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 Genomes 7:323–335Eduardo I, Chietera G, Pirona R, Pacheco I, Troggio M, Banchi E, Bassi D, Rossini L, Vecchietti A, Pozzi C (2013) Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps. Tree Genet Genomes 9:189–204Eduardo I, López-Girona E, BatlIe I, Reig G, Iglesias I, Howad W, Arús P, Aranzana MJ (2014) Development of diagnostic markers for selection of the subacid trait in peach. Tree Genet Genomes 10:1695–1709Eduardo I, Picañol R, Rojas E, BatlIe I, Howad W, Aranzana MJ, Arús P (2015) Mapping of a major gene for the slow ripening character in peach: co-location with the maturity date gene and development of a candidate gene-based diagnostic marker for its selection. Euphytica 205:627–636Etienne C, Rothan C, Moing A, Plomion C, Bodénès C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159FAOSTAT (2015) Food and Agriculture Organization of the United Nations. http://faostat.fao.org/site/291/default.aspx . Accessed 1 August 2015Font i Forcada C, Oraguzie N, Igartua E, Moreno MA, Gogorcena Y (2013) Population structure and marker-trait associations for pomological traits in peach and nectarine cultivars. Tree Genet Genomes 9:331–349Fresnedo-Ramírez J, Bink MCAM, van der Weg E, Famula TR, Crisosto CH, Frett TJ, Gasic K, Peace CP, Gradziel TM (2015) QTL mapping of pomological traits in peach and related species breeding germplasm. Mol Breed 35:166Frett T, Reighard G, Okie W, Gasic K (2014) Mapping quantitative trait loci associated with blush in peach [Prunus persica (L.) Batsch]. Tree Genet Genomes 10:367–381GDR (2015) Genome database for Rosaceae. http://www.rosaceae.org/species/prunus_persica/genome_v1.0 . Accessed 13 Nov 2015Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137Illa 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(4):667–682Infante R, Farcuh M, Meneses C (2008) Monitoring the sensorial quality and aroma through an electronic nose in peaches during cold storage. J Sci Food Agric 88:2073–2078Jáuregui B, De Vicente MC, Messeguer R, Felipe A, Bonnet A, Salesses G, Arús P (2001) A reciprocal translocation between ‘Garfi’ almond and ‘Nemared’ peach. Theor Appl Genet 102:1169–1176Martin C, Zhang Y, Tonelli C, Petroni K (2013) Plants, diet, and health. Annu Rev Plant Biol 64:19–46Martínez-García PJ, Fresnedo-Ramírez J, Parfitt DE, Gradziel TM, Crisosto CH (2013a) Effect prediction of identified SNPs linked to fruit quality and chilling injury in peach [Prunus persica (L.) Batsch]. Plant Mol Biol 81:161–174Martínez-García PJ, Parfitt DE, Ogundiwin EA, Fass J, Chan HM, Ahmad R, Lurie S, Dandekar A, Gradziel TM, Crisosto CH (2013b) High density SNP mapping and QTL analysis for fruit quality characteristics in peach (Prunus persica L.). Tree Genet Genomes 9:19–36Nielsen R, Hubisz MJ, Clark AG (2004) Reconstituting the frequency spectrum of ascertained single-nucleotide polymorphism data. Genetics 168:2373–2382Nuñez-Lillo G, Cifuentes-Esquivel A, Troggio M, Micheletti D, Rodrigo Infante R, Campos-Vargas R, Orellana A, Blanco-Herrera F, Meneses C (2015) Identification of candidate genes associated with mealiness and maturity date in peach [Prunus persica (L.) Batsch] using QTL analysis and deep sequencing. Tree Genet Genomes 1:86Ogundiwin EA, Peace CP, Gradziel TM, Parfitt DE, Bliss FA, Crisosto CH (2009) A fruit quality gene map of Prunus. BMC Genomics 10:587Orazem P, Stampar F, Hudina M (2011) Quality analysis of ‘Redhaven’ peach fruit grafted on 11 rootstocks of different genetic origin in a replant soil. Food Chem 124(4):1691–1698Pacheco I, Bassi D, Eduardo I, Ciacciulli A, Pirona R, Rossini L, Vecchietti A (2014) QTL mapping for brown rot (Monilinia fructigena) resistance in an intraspecific peach (Prunus persica L. Batsch) F1 progeny. Tree Genet Genomes 10:1223–1242. doi: 10.1007/s11295-014-0756-7Peace C, Norelli J (2009) Genomics approaches to crop improvement in the Rosaceae. In: Folta KM, Gardiner SE (eds) Genetics and genomics of Rosaceae, vol 6. Plant genetics and genomics: crops and models. Springer, New York, pp 19–53Pirona R, Eduardo I, Pacheco I, Da Silva Linge C, Miculan M, Verde I, Tartarini S, Dondini L, Giorgio Pea G, Daniele Bassi D, Rossini L (2013) Fine mapping and identification of a candidate gene for a major locus controlling maturity date in peach. BMC Plant Biol 3:166Quarta R, Dettori MT, Sartori A, Verde I (2000) Genetic linkage map and QTL analysis in peach. Acta Hortic 521:233–242Quilot B, Wu BH, Kervella J, Génard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897Romeu J, Monforte AJ, Sánchez G, Granell A, García-Brunton J, Badenes M, Ríos G (2014) Quantitative trait loci affecting reproductive phenology in peach. BMC Plant Biol 14:52Ru S, Main D, Evans K, Peace C (2015) Current applications, challenges, and perspectives of marker-assisted seedling selection in Rosaceae tree fruit breeding. Tree Genet Genomes 11:8Salazar JA, Ruiz D, Egea J, Martínez-Gómez P (2013) Transmission of fruit quality traits in apricot (Prunus armeniaca L.) and analysis of linked quantitative trait loci (QTLs) using simple sequence repeat (SSR) markers. Plant Mol Biol Rep 31:1506–1517. doi: 10.1007/s11105-013-0625-9Sánchez G, Besada C, Badenes ML, Monforte AJ, Granell A (2012) A non-targeted approach unravels the volatile network in peach fruit. PLoS One 7(6), e38992Sánchez G, Romeu J, García J, Monforte AJ, Badenes M, Granell A (2014) The peach volatilome modularity is reflected at the genetic and environmental response levels in a QTL mapping population. BMC Plant Biology 14:137Steemers FJ, Chang W, Lee G, Barker DL, Shen R, Gunderson KL (2006) Whole-genome genotyping with the single-base extension assay. Nat Methods 3(1):31–33. doi: 10.1038/nmeth842Van Ooijen JW (1992) Accuracy of mapping quantitative trait loci in autogamous species. Theor Appl Genet 84:803–811Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., Wageningen, NetherlandsVerde I, Quarta R, Cedrola C, Dettori MT (2002) QTL analysis of agronomic traits in a BC1 peach population. Acta Hortic 592:291–297Verde I, Bassil N, Scalabrin S, Gilmore B, Lawley CT, Gasic K, Micheletti D, Rosyara UR, Cattonaro F, Vendramin E, Main D, Aramini V, Blas AL, Mockler TC, Bryant DW, Wilhelm L, Troggio M, Sosinski B, Aranzana MJ, Arús P, Iezzoni A, Morgante M, Peace C (2012) Development and evaluation of a 9k SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PLoS One 7(4), e35668Verde I, Abbott AG, Scalabrin S, Jung S, Shu SQ, Marroni F, Zhebentyayeva T, et al. (Int Peach Genome I) (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487-U447Verdu CF, Guyot S, Childebrand N, Bahut M, Celton JM, Gaillard S, Lasserre-Zuber P, Troggio M, Guilet D, Laurens F (2014) QTL analysis and candidate gene mapping for the polyphenol content in cider apple. PLoS One 9(10), e107103Vizzotto M, Porter W, Byrne D, Luis Cisneros-Zevallos L (2014) Polyphenols of selected peach and plum genotypes reduce cell viability and inhibit proliferation of breast cancer cells while not affecting normal cells. Food Chem 164:363–370Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78Wargovich MJ, Morris J, Moseley V, Weber R, Byrne DH (2012) Developing fruit cultivars with enhanced health properties, in fruit breeding. In: Badenes ML, Byrne DH (eds) Fruit breeding, vol 8, Handbook of plant breeding. Springer, New York, pp 37–68Yang J, Hu Ch, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24(5):721–723Yang N, Reighard G, Ritchie D, Okie W, Gasic K (2013) Mapping quantitative trait loci associated with resistance to bacterial spot (Xanthomonas arboricola pv. pruni) in peach. Tree Genet Genomes 9:573–586Zeballos J (2012) Identification of genomic region related to fruit quality traits in peach. Universidad de Lleida, Zaragoza, SpainZeballos J, Abidi W, Giménez R, Monforte AJ, Moreno MA, Gogorcena Y (2015) QTL analysis of fruit quality traits in peach [Prunus persica (L.) Batsch] using dense SNP maps. Acta Hortic 1084:703–710Zhebentyayeva TN, Swire-Clark G, Georgi LL, Garay L, Jung S, Forrest S, Blenda AV, Blackmon B, Mook J, Horn R, Howad W, Arús P, Main D, Tomkins JP, Sosinski B, Baird WV, Reighard GL, Abbott AG (2008) A framework physical map for peach, a model Rosaceae species. Tree Genet Genomes 4:745–756Zhebentyayeva TN, Fan S, Chandra A, Bielenberg DG, Reighard GL, Okie WR, Abbott AG (2014) Dissection of chilling requirement and bloom date QTLs in peach using a whole genome sequencing of sibling trees from an F2 mapping population. Tree Genet Genomes 10:35–5