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Molecular-level and trait-level differentiation between the cultivated apple (Malus× domestica Borkh.) and its main progenitor Malus sieversii

  • Satish Kumar (a1), Pierre Raulier (a2), David Chagné (a3) and Claire Whitworth (a1)

Abstract

The present study is the first to compare the trait-level differentiation (Q st) and the molecular-level differentiation (F st) between Malus× domestica and Malus sieversii. A set of 115 accessions representing M.× domestica (99) and M. sieversii (16) were genotyped using the International RosBREED SNP Consortium apple 8K SNP array and phenotyped for eight fruit quality traits in a clonally replicated experiment. A set of 3521 single nucleotide polymorphisms (SNPs) with an average call rate of 98% was retained following SNP data quality filters. About 86% of the total SNPs were polymorphic in M. sieversii, while all but three SNPs were polymorphic in M. × domestica. The patterns of linkage disequilibrium were different, especially at the longer distances, between the two species. No differentiation (F st= 0) was observed for nearly 23% of the SNPs, but about 20% of the SNPs exhibited a high genetic differentiation (F st≥ 0.15). A highly significant (P< 0.001) genome-level F st= 0.12 was observed between M. × domestica and M. sieversii. The average estimated Q st value was 0.20 (range 0.08–0.40), and for three of the eight studied traits (crispness, flavour intensity and fruit weight), Q st value was more than twice the estimated genome-level F st value. A higher Q st value than F st value for four of the eight fruit quality traits indicated differential (or directional) selection for these traits in M. × domestica. The average posterior probability of assignment of M. × domestica accessions to the M. sieversii gene pool was 11%, supporting the hypothesis of M. sieversii being one of the progenitors of the domesticated apple.

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Corresponding author

* Corresponding author. E-mail: satish.kumar@plantandfood.co.nz

References

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Allendorf, FW and Seeb, LW (2000) Concordance of genetic divergence among sockeye salmon populations at allozyme, nuclear DNA, and mitochondrial DNA markers. Evolution 54: 640651.
Brookfield, P, Murphy, P, Harker, R and MacRae, E (1997) Starch degradation and starch pattern indices; interpretation and relationship to maturity. Postharvest Biology and Technology 11: 2330.
Brown, AG (1975) Apples. In: Janick, J and Moore, JN (eds) Advances in Fruit Breeding. West Lafayette, IN: Purdue University Press, pp. 337.
Browning, SR and Browning, BL (2007) Rapid and accurate haplotype phasing and missing data inference for whole genome association studies using localized haplotype clustering. American Journal of Human Genetics 81: 10841097.
Chagné, D, Carlisle, C, Blond, C, Volz, RK, Whitworth, C, Oraguzie, NZ, Crowhurst, RN, Allan, AC, Espley, RV, Hellens, RP and Gardiner, SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8: 212.
Chagné, D, Crowhurst, RN, Troggio, M, Davey, MW, Gilmore, B, Lawley, C, Vanderzande, S, Hellens, RP, Kumar, S, Cestaro, A, Velasco, R, Main, D, Rees, JD, Iezzoni, A, Mockler, T, Wilhelm, L, van de Weg, E, Gardiner, SE, Bassil, N and Peace, C (2012) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One 7: e31745.
Chapman, C (1989) Principles of germplasm evaluation. In: Stalker, HT and Chapman, C (eds) IBPGR Training Courses: Lecture Series 2. Scientific Management of Germplasm: Characterization, Evaluation, and Enhancement. Rome: International Board for Plant Genetic Resources, pp. 5564.
Clegg, MT (1990) Molecular diversity in plant populations. In: Brown, AHD, Clegg, MT, Kahler, AL and Weir, BS (eds) Plant Population Genetics, Breeding, and Genetic Resources. Sunderland, MA: Sinauer Associates, Inc., pp. 98115.
Coart, E, Van Glabeke, S, De Loose, M, Larsen, AS and Roldan-Ruiz, I (2006) Chloroplast diversity in the genus Malus: new insights into the relationship between the European wild apple (Malus sylvestris (L.) Mill.) and the domesticated apple (Malus domestica Borkh.). Molecular Ecology 15: 21712182.
Cockerham, CC and Weir, BS (1993) Estimation of gene flow from F-statistics. Evolution 47: 855863.
Cornille, A, Gladieux, P, Smulders, MJM, Roldan-Ruiz, I, Laurens, F, Le Cam, B, Nersesyan, A, Clavel, J, Olonova, M, Feugey, L, Gabrielyan, I, Zhang, X-G, Tenaillon, MI and Giraud, T (2012) New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated Varieties. PLoS Genetics 8: e1002703.
Doebley, J (1989) Isozymic evidence and the evolution of crop plants. In: Soltis, DE and Soltis, PS (eds) Isozymes in Plant Biology. Portland, OR: Dioscorides Press, pp. 165191.
Dunemann, F, Kahnau, R and Schmidt, H (1994) Genetic relationships in Malus evaluated by RAPD ‘fingerprinting’ of cultivars and wild species. Plant Breeding 113: 150159.
Espley, RV, Hellens, RP, Putterill, J, Stevenson, DE, Kutty-Amma, S and Allan, AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant Journal 49: 414427.
Foll, M and Gaggiotti, O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180: 977993.
Forsline, PL and Aldwinckle, HS (2004) Evaluation of Malus sieversii seedling populations for disease resistance and horticultural traits. Acta Horticulturae 663: 529534.
Frankham, R (1999) Quantitative genetics in conservation biology. Genetic Resources 74: 37244.
Gharghani, A, Zamani, Z, Talaie, A, Oraguzie, NC, Fatahi, R, Hajnajari, H, Wiedow, C and Gardiner, SE (2009) Genetic identity and relationships of Iranian apple (Malus× domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genetic Resources and Crop Evolution 56: 829842.
Gilmour, AR, Cullis, BR, Harding, SA and Thompson, R (2006) ASReml Update: What's New in Release 2.00. Hemel Hempstead: VSN International Limited.
Gross, BL, Henk, AD, Forsline, PL, Richards, CM and Volk, GM (2012) Identification of interspecific hybrids among domesticated apple and its wild relatives. Tree Genetics and Genomes 8: 12231235.
Harris, SA, Robinson, JP and Juniper, BE (2002) Genetic clues to the origin of the apple. Trends in Genetics 18: 426430.
Harrison, N and Harrison, R (2011) On the evolutionary history of the domesticated apple. Nature Genetics 43: 10431044.
Helyar, SJ, Hemmer-Hansen, J, Bekkevold, D, Taylor, MI, Ogden, R, Limborg, MT, Cariani, A, Maes, GE, Diopere, E, Carvalho, GR and Nielsen, EE (2011) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Molecular Ecology Resources 11: 123136.
Hill, WG and Robertson, A (1968) Linkage disequilibrium in finite populations. Theoretical and Applied Genetics 38: 226231.
Hilu, KW (1989) Taxonomy of cultivated plants. In: Stalker, HT and Chapman, C (eds) IBPGR Training Courses: Lecture Series 2. Scientific Management of Germplasm: Characterization, Evaluation, and Enhancement. Rome: International Board for Plant Genetic Resources, pp. 3340.
Hokanson, SC, Szewc-McFadden, AK, Lamboy, WF and McFerson, JR (1998) Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus domestica Borkh. core subset collection. Theoretical and Applied Genetics 97: 671683.
Kaeuffer, R, Reale, D, Coltman, DW and Pontier, D (2007) Detecting population structure using STRUCTURE software: effect of background linkage disequilibrium. Heredity 99: 374380.
Khan, SA, Beekwilder, J, Schaart, JG, Mumm, R, Soriano, JM, Jacobsen, E and Schouten, HJ (2013) Differences in acidity of apples are probably mainly caused by a malic acid transporter gene on LG16. Tree Genetics and Genomes 9: 475487.
Kirk, H and Freeland, JR (2011) Applications and implications of neutral versus non-neutral markers in molecular ecology. International Journal of Molecular Sciences 12: 39663988.
Kumar, SK, Volz, RK, Alspach, PA and Bus, VGM (2010) Development of a recurrent apple breeding programme in New Zealand: a synthesis of results, and a proposed revised breeding strategy. Euphytica 173: 207222.
Kumar, S, Chagné, D, Bink, MCAM, Volz, RK, Whitworth, C and Charmaine, C (2012) Genomic selection for fruit quality traits in apple (Malus× domestica Borkh.). PLoS One 7: e36674.
Kumar, S, Garrick, DG, Bink, MCAM, Whitworth, C, Chagné, D and Volz, RK (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomic 14: 93.
Larsen, AS, Asmussen, CB, Coart, E, Olrik, DC and Kjaer, ED (2006) Hybridization and genetic variation in Danish populations of European crab apple (Malus sylvestris). Tree Genetics and Genomes 2: 8697.
Leberg, PL (2002) Estimating allelic richness: effects of sample size and bottleneck. Molecular Ecology 11: 24452449.
Lin-Wang, K, Micheletti, D, Palmer, J, Volz, R, Lozano, L, Espley, R, Hellens, RP, Chagne, D, Rowan, DD, Troggio, M, Iglesias, I and Allan, A (2011) High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant and Cell Environment 34: 11761190.
Lipka, AE, Tian, F, Wang, Q, Peiffer, J, Li, M, Bradbury, PJ, Gore, MA, Buckler, ES and Zhang, Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28: 23972399.
Liu, N, Chen, L, Wang, S, Oh, C and Zhao, H (2005) Comparison of single nucleotide polymorphisms and microsatellites in inference of population structure. BMC Genetics 6: S26.
Luby, JJ, Alspach, PA, Bus, VGM and Oraguzie, NC (2002) Field resistance to fire blight in a diverse apple (Malus sp.) germplasm collection. Journal of American Society of Horticultural Science 127: 245253.
Lynch, M and Walsh, B (1998) Genetics and Analysis of Quantitative Traits. Sunderland, MA: Sinauer Associates.
Mangin, B, Siberchicot, A, Nicolas, S, Doligez, A, This, P and Cierco-Ayrolles, C (2012) Novel measures of linkage disequilibrium that corrects the bias due to population structure and relatedness. Heredity 108: 285291.
McKay, JK and Latta, RG (2002) Adaptive population divergence: markers, QTL and traits. Trends in Ecology and Evolution 17: 285291.
Merilä, J and Crnokrak, P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. Journal of Evolutionary Biology 14: 92103.
Micheletti, D, Troggio, M, Zharkikh, A, Costa, F, Malnoy, M, Velasco, R and Salvi, S (2011) Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genetics and Genomes 7: 857868.
Myles, S, Peiffer, J, Brown, PJ, Ersoz, ES, Zhang, Z, Costich, DE and Buckler, ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21: 21942202.
Nielsen, EE, Hansen, MM and Meldrup, D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in non-model organisms. Molecular Ecology 15: 32193229.
Noiton, DAM, Hofstee, M, Alspach, PA, Brewer, L and Howard, C (1999) Increasing genetic diversity for apple breeding: a preliminary report. Acta Horticulturae 484: 105107.
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945959.
Ritland, K (2000) Marker-inferred relatedness as a tool for detecting heritability in nature. Molecular Ecology 9: 11951204.
Robinson, JP, Harris, SA and Juniper, BE (2001) Taxonomy of the genus Malus Mill. (Rosaceae) with emphasis on the cultivated apple, Malus × domestica Borkh. Plant Systematics and Evolution 226: 3558.
Røen, D, Ekholm, A and Rumpunen, K (2009) Estimating useful diversity in the Norwegian core collection of apples. Acta Horticulturae 814: 131136.
Rousset, F (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103106.
Spitze, K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozyme variation. Genetics 135: 367374.
Van Raden, PM (2008) Efficient methods to compute genomic predictions. Journal of Dairy Science 91: 44144423.
Van Treuren, R, Kemp, H, Ernsting, G, Jongejans, B, Houtman, H and Visser, L (2010) Microsatellite genotyping of apple (Malus × domestica Borkh.) genetic resources in the Netherlands: application in collection management and variety identification. Genetic Resources and Crop Evolution 57: 853865.
Velasco, R, Zharkikh, A, Affourtit, J, Dhingra, A, Cestaro, A, Kalyanaraman, A, Fontana, P, Bhatnagar, SK, Troggio, M, Pruss, D, Salvi, S, Pindo, M, Baldi, P, Castelletti, S, Cavaiuolo, M, Coppola, G, Costa, F, Cova, V, Dal Ri, A, Goremykin, V, Komjanc, M, Longhi, S, Magnago, P, Malacarne, G, Malnoy, M, Micheletti, D, Moretto, M, Perazzolli, M, Si-Ammour, A, Vezzulli, S, Zini, E, Eldredge, G, Fitzgerald, LM, Gutin, N, Lanchbury, J, Macalma, T, Mitchell, JT, Reid, J, Wardell, B, Kodira, C, Chen, Z, Desany, B, Niazi, F, Palmer, M, Koepke, T, Jiwan, D, Schaeffer, S, Krishnan, V, Wu, C, Chu, VT, King, ST, Vick, J, Tao, Q, Mraz, A, Stormo, A, Stromo, K, Bogden, R, Ederle, D, Stella, A, Vecchietti, A, Kater, MM, Masiero, S, Lasserre, P, Lespinasse, Y, Allan, AC, Bus, V, Chagné, D, Crowhurst, RN, Gleave, AP, Lavezzo, E, Fawcett, JA, Proost, S, Rouzé, P, Sterck, L, Toppo, S, Lazzari, B, Hellens, RP, Durel, CE, Gutin, A, Bumgarner, RE, Gardiner, SE, Skolnick, M, Egholm, M, Van de Peer, Y, Salamini, F and Viola, R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42: 833839.
Weir, BS and Cockerham, CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 13581370.
Whitlock, MC (1999) Neutral additive genetic variance in a metapopulation. Genetic Resources 74: 215221.
Xu, K, Wang, A and Brown, S (2012) Genetic characterization of the Ma locus with pH and titratable acidity in apple. Molecular Breeding 30: 899912.
Yan, G, Long, H, Song, W and Chen, R (2008) Genetic polymorphism of Malus sieversii populations in Xinjiang, China. Genetic Resources and Crop Evolution 55: 171181.
Yu, J, Pressoir, G, Briggs, WH, Vroh-Bi, I, Yamasaki, M, Doebley, JF, McMullen, MD, Gaut, BS, Nielsen, DM, Holland, JB, Kresovich, S and Buckler, ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38: 203208.

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Molecular-level and trait-level differentiation between the cultivated apple (Malus× domestica Borkh.) and its main progenitor Malus sieversii

  • Satish Kumar (a1), Pierre Raulier (a2), David Chagné (a3) and Claire Whitworth (a1)

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