Genomic basis of the differences between cider and dessert apple varieties

Abstract

Unraveling the genomic processes at play during variety diversification is of fundamental interest for understanding evolution, but also of applied interest in crop science. It can indeed provide knowledge on the genetic bases of traits for crop improvement and germplasm diversity management. Apple is one of the most important fruit crops in temperate regions, having both great economic and cultural values. Sweet dessert apples are used for direct consumption, while bitter cider apples are used to produce cider. Several important traits are known to differentiate the two variety types, in particular fruit size, biennial versus annual fruit bearing, and bitterness, caused by a higher content in polyphenols. Here, we used an Illumina 8k SNP chip on two core collections, of 48 dessert and 48 cider apples, respectively, for identifying genomic regions responsible for the differences between cider and dessert apples. The genome-wide level of genetic differentiation between cider and dessert apples was low, although 17 candidate regions showed signatures of divergent selection, displaying either outlier F_ST values or significant association with phenotypic traits (bitter versus sweet fruits). These candidate regions encompassed 420 genes involved in a variety of functions and metabolic pathways, including several colocalizations with QTLs for polyphenol compounds.

Literature cited Alexander, D. H., J. Novembre, and K. Lange 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research. 19:1655–1664. Alonso-Blanco, C., and B. Méndez-Vigo 2014. Genetic architecture of naturally occurring quantitative traits in plants: an updated synthesis. Current Opinion in Plant Biology 18:37–43. Axelsson, E., A. Ratnakumar, M. L. Arendt, K. Maqbool, M. T. Webster, M. Perloski, O. Liberg et al. 2013. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495:360–364. Barrett, J. C., B. Fry, J. Maller, and M. J. Daly 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265. Beaumont, M. A., and D. J. Balding 2004. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 13:969–980. Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste, and F. Bonhomme 1996–2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France. Boré, J. M., and J. Fleckinger 1997. Pommiers à cidre (variétés de France). Brown, G. R., G. P. Gill, R. J. Kuntz, C. H. Langley, and D. B. Neale 2004. Nucleotide diversity and linkage disequilibrium in loblolly pine. Proceedings of the National Academy of Sciences of the United States of America 101:15255–15260. Calenge, F., A. Faure, M. Goerre, C. Gebhardt, W. E. Van de Weg, L. Parisi, and C. E. Durel 2004. Quantitative Trait Loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379. del Campo, G., J. I. Santos, I. Berregi, and A. Munduate 2005. Differentiation of Basque cider apple juices from different cultivars by means of chemometric techniques. Food Control 16:549–555. Camus-Kulandaivelu, L., L. M. Chevin, C. Tollon-Cordet, A. Charcosset, D. Manicacci, and M. I. Tenaillon 2008. Patterns of molecular evolution associated with two selective sweeps in the Tb1–Dwarf8 region in maize. Genetics 180:1107–1121. Celton, J. M., S. Martinez, M. J. Jammes, A. Bechti, S. Salvi, J. M. Legave, and E. Costes 2011. Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. The New Phytologist 192:378–392. Chagne, D., R. N. Crowhurst, M. Troggio, M. W. Davey, B. Gilmore, C. Lawley, S. Vanderzande et al. 2012a. Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS ONE 7:e31745. Chagne, D., C. Krieger, M. Rassam, M. Sullivan, J. Fraser, C. André, M. Pindo et al. 2012b. QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biology 12:1–16. Collard, B. C. Y., and D. J. Mackill 2008. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences 363:557–572. Conesa, A., S. Götz, J. M. García-Gómez, J. Terol, M. Talón, and M. Robles 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. Cornille, A., T. Giraud, M. J. Smulders, I. Roldan-Ruiz, and P. Gladieux 2014. The domestication and evolutionary ecology of apples. Trends in Genetics 30:57–65. Cornille, A., P. Gladieux, M. J. M. Smulders, I. Roldán-Ruiz, F. Laurens, B. Le Cam, A. Nersesyan et al. 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. Dapena, E., M. Minarro, and M. D. Blazquez 2005. Organic cider-apple production in Asturias (NW Spain). IOBC wprs Bulletin 28:161. Darwin, C. 1987. 1856. Charles darwin?s natural selection. In: R. C. Stauffer, ed. Species. Cambridge University Press, Cambridge. Douglas, G. L., and T. R. Klaenhammer 2010. Genomic evolution of domesticated microorganisms. Annual Review of Food Science and Technology 1:397–414. Foll, M., and O. Gaggiotti 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993. Gallavotti, A., Q. Zhao, J. Kyozuka, R. B. Meeley, M. K. Ritter, J. F. Doebley, M. E. Pe et al. 2004. The role of barren stalk1 in the architecture of maize. Nature 432:630–635. Guitton, B., J. J. Kelner, R. Velasco, S. E. Gardiner, D. Chagne, and E. Costes 2012. Genetic control of biennial bearing in apple. Journal of Experimental Botany 63:131–149. Ingvarsson, P. K. 2005. Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953. Iwata, H., T. Hayashi, S. Terakami, N. Takada, Y. Sawamura, and T. Yamamoto 2013. Potential assessment of genome-wide association study and genomic selection in Japanese pear Pyrus pyrifolia. Breeding Science 63:125–140. Janick, J. 2005. The origins of fruits, fruit growing, and fruit breeding. In J. Janick, ed. Plant Breeding Reviews, pp. 255–322. John Wiley & Sons, Inc, Hoboken, NJ. Jugdé, H., D. Nguy, I. Moller, J. M. Cooney, and R. G. Atkinson 2008. Isolation and characterization of a novel glycosyltransferase that converts phloretin to phlorizin, a potent antioxidant in apple. FEBS journal 275:3804–3814. Juniper, B. E., and D. J. Mabberley 2006. The Story of the Apple. Timber Press, Portland, OR. Khan, S. A., J. Schaart, J. Beekwilder, A. Allan, Y. Tikunov, E. Jacobsen, and H. Schouten 2012a. The mQTL hotspot on linkage group 16 for phenolic compounds in apple fruits is probably the result of a leucoanthocyanidin reductase gene at that locus. BMC Research Notes 5:618. Khan, S. A., P.-Y. Chibon, R. C. H. de Vos, B. A. Schipper, E. Walraven, J. Beekwilder, T. van Dijk et al. 2012b. Genetic analysis of metabolites in apple fruits indicates an mQTL hotspot for phenolic compounds on linkage group 16. Journal of Experimental Botany 63:2895–2908. Kumar, S., D. Chagné, M. C. A. M. Bink, R. K. Volz, C. Whitworth, and C. Carlisle 2012. Genomic selection for fruit quality traits in apple (Malus×domestica Borkh.). PLoS ONE 7:e36674. Lachance, J., and S. A. Tishkoff 2013. SNP ascertainment bias in population genetic analyses: why it is important, and how to correct it. BioEssays 35:780–786. Larson, G., and J. Burger 2013. A population genetics view of animal domestication. Trends in Genetics 29:197–205. Lea, A. G. H., and J. R. Piggott 2003. Fermented Beverage Production, 2nd edn. Kluwer Academic/Plenum Publishers, New York. Lespinasse, Y., and J. P. Paulin 1990. Apple breeding programme for fire blight resistance: strategy used and first results. Acta Horticulturae (ISHS) 273:285–296. Li, X. W., X. Q. Meng, H. J. Jia, M. L. Yu, R. J. Ma, L. R. Wang, K. Cao et al. 2013. Peach genetic resources: diversity, population structure and linkage disequilibrium. BMC Genetics 14:84. Longhi, S., M. Moretto, R. Viola, R. Velasco, and F. Costa 2012. Comprehensive QTL mapping survey dissects the complex fruit texture physiology in apple (Malus x domestica Borkh.). Journal of Experimental Botany 63:1107–1121. Maenhout, S., B. De Baets, and G. Haesaert 2009. CoCoa: a software tool for estimating the coefficient of coancestry from multilocus genotype data. Bioinformatics 25:2753–2754. Mangin, B., A. Siberchicot, S. Nicolas, A. Doligez, P. This, and C. Cierco-Ayrolles 2012. Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity 108:285–291. McTavish, E. J., J. E. Decker, R. D. Schnabel, J. F. Taylor, and D. M. Hillis 2013. New World cattle show ancestry from multiple independent domestication events. Proceedings of the National Academy of Sciences of the United States of America 110:E1398–E1406. Meyer, R. S., A. E. DuVal, and H. R. Jensen 2012. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. The New Phytologist 196:29–48. Micheletti, D., F. Costa, P. Baldi, M. Troggio, M. Pindo, M. Komjanc, M. Malnoy et al. 2008. Linkage disequilibrium analysis to enable more efficient gene and QTL mapping in apple. RGC4. Morgan, J., A. Richards, and E. Dowle 2002. The New Book of Apples: the Definitive Guide to Apples, Including Over 2000 Varieties. Ebury, London. Nielsen, R. 2004. Population genetic analysis of ascertained SNP data. Human genomics 1:218–224. Nielsen, R., and J. Signorovitch 2003. Correcting for ascertainment biases when analyzing SNP data: applications to the estimation of linkage disequilibrium. Theoretical Population Biology 63:245–255. Nordborg, M., and S. Tavare 2002. Linkage disequilibrium: what history has to tell us. Trends in Genetics 18:83–90. Palaisa, K. A., M. Morgante, M. Williams, and A. Rafalski 2003. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. The Plant Cell 15:1795–1806. Paulin, J. P., G. Lachaud, R. Chartier, and J. M. Bore 1988. Sensibilité au feu bactérien de variétés de pommiers à cidre. Résultats de 3 années d'expérimentation.35. Pe'er, I., Y. R. Chretien, P. I. de Bakker, J. C. Barrett, M. J. Daly, and D. M. Altshuler 2006. Biases and reconciliation in estimates of linkage disequilibrium in the human genome. American Journal of Human Genetics 78:588–603. Pereira-Lorenzo, S., A. M. Ramos-Cabrer, and M. Fischer 2009. Breeding Apple (Malus x Domestica Borkh). In: S. M Jain and P. M. Priyadarshan, eds. Breeding Plantation Tree Crops: Temperate Species. pp. 33–81. Springer, New York. Perrier, X., A. Flori, and F. Bonnot 2003. Data analysis methods. In P. Hamon, M. Seguin, X. Perrier, and J. C. Glaszmann, eds. Genetic Diversity of Cultivated Tropical Plants. pp. 43–76. Science Publishers, Inc., Montpellier, France. Perrier, X., and J. P. Jacquemoud-Collet 2006. DARwin software v. 6.0.010. http://darwin.cirad.fr/. (accessed on 21 April 2015). Prada, D. 2009. Molecular population genetics and agronomic alleles in seed banks: searching for a needle in a haystack? Journal of Experimental Botany 60:2541–2552. Sanoner, P., S. Guyot, N. Marnet, D. Molle, and J. P. Drilleau 1999. Polyphenol profiles of French cider apple varieties (Malus domestica sp.). Journal of Agricultural and Food Chemistry 47:4847–4853. Scheet, P., and M. Stephens 2006. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. American Journal of Human Genetics 78:629–644. Segura, V., C. Cilas, and E. Costes 2008. Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: mixed linear modelling of repeated spatial and temporal measures. The New Phytologist 178:302–314. Soller, M. 1994. Marker assisted selection – an overview. Animal Biotechnology 5:193–207. Turner, S. D. 2014. qqman: An R Package for Visualizing GWAS Results Using Q-Q and Manhattan Plots (http://biorxiv.org). Velasco, R., A. Zharkikh, J. Affourtit, A. Dhingra, A. Cestaro, A. Kalyanaraman, P. Fontana et al. 2010. The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genetics 42:833–839. Verdu, C. F., S. Guyot, N. Childebrand, M. Bahut, J. M. Celton, S. Gaillard, P. Lasserre-Zuber et al. 2014. QTL analysis and candidate gene mapping for the polyphenol content in cider apple. PLoS ONE 9:e107103. Volk, G. M., C. T. Chao, J. Norelli, S. K. Brown, G. Fazio, C. Peace, J. McFerson et al. 2014. The vulnerability of US apple (Malus) genetic resources. Genetic Resources and Crop Evolution 1–30. Walsh, B. 2008. Using molecular markers for detecting domestication, improvement, and adaptation genes. Euphytica 161:1–17. Wang, H., T. Nussbaum-Wagler, B. Li, Q. Zhao, Y. Vigouroux, M. Faller, K. Bomblies et al. 2005. The origin of the naked grains of maize. Nature 436:714–719. Wang, R. L., A. Stec, J. Hey, L. Lukens, and J. F. Doebley 1999. The limits of selection during maize domestication. Nature 398:236–239. Whiting, G. C., and R. A. Coggins 1975. Estimation of the monomeric phenolics of ciders. Journal of the Science of Food and Agriculture 26:1833–1838. Whitt, S. R., L. M. Wilson, M. I. Tenaillon, B. S. Gaut, and E. S. Buckler 2002. Genetic diversity and selection in the maize starch pathway. Proceedings of the National Academy of Sciences 99:12959–12962. Yamasaki, M., M. I. Tenaillon, I. V. Bi, S. G. Schroeder, H. Sanchez-Villeda, J. F. Doebley, B. S. Gaut et al. 2005. A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. The Plant Cell 17:2859–2872. Yuan, J. H., A. Cornille, T. Giraud, F. Y. Cheng, and Y. H. Hu 2014. Independent domestications of cultivated tree peonies from different wild peony species. Molecular Ecology 23:82–95. Zhou, X., and M. Stephens 2012. Genome-wide efficient mixed-model analysis for association studies. Nature Genetics 44:821–824. Zhou, X., P. Carbonetto, and M. Stephens 2013. Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genetics 9:e1003264.