Genetic diversity, population structure, and relationships of apricot (Prunus) based on restriction site-associated DNA sequencing

Abstract

Single-nucleotide polymorphisms (SNPs) are the most abundant form of genomic polymorphisms and are widely used in population genetics research. Here, high-throughput sequencing was used to examine the genome-level diversity, population structure, and relationships of apricot, which are important for germplasm conservation and molecular breeding. Restriction site-associated DNA sequencing (RAD-seq) was adopted to sequence 168 Prunus spp. accessions distributed in five ecological groups, including 74 accessions of cultivated Prunus armeniaca L. and 94 accessions of wild apricots (P. armeniaca L. and Prunus sibirica L.), which generated 417,961 high-quality SNPs. We used cluster, genetic structure, and principal component analyses to examine the genetic diversities and genetic relationships of the 168 accessions. The Dzhungar-Ili ecological group accessions showed the highest genetic diversity in terms of private allele number, observed heterozygosity, and nucleotide diversity. We speculate that the Central Asian ecological group accessions were domesticated from the Dzhungar-Ili ecological group accessions. The population structure and gene flow of the North China and European ecological group accessions suggested a genetic background of P. sibirica. We argue that the two groups should be considered hybrid swarms connected to P. sibirica by continuous and extensive gene flow. P. armeniaca originated in Northwest China (Ili Valley), subsequently spread throughout Central Asia, and eventually spread to Europe. In addition, selective sweep signatures in P. armeniaca during domestication from wild to cultivated apricots, combined with differentially expressed genes, underlie distinct fruit traits, including sugars, aromas, organic acids, and carotenoids. This study provides substantive and valuable genomic resources that will significantly advance apricot improvement and effective utilization.

References

[1] Romero, C., Pedryc, A., Munoz, V., Llacer, G. & Badenes, M. L. Genetic diversity of different apricot geographical groups determined by SSR markers. Genome 46, 244-252 (2003).

[2] Rehder, A. Manual of Cultivated Trees and Shrubs Hardy in North America, Exclusive of the Subtropical and Warmer Temperate Regions (Macmillan, New York, 1940).

[3] Bortiri, E. et al. Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF Spacer DNA. Syst. Bot. 26, 797-807 (2001).

[4] Folta, K. M. & Gardiner, S. E. in Genetics and Genomics of Rosaceae, Genomics-Based Opportunities in Apricot (eds Folta, K. M. & Gardiner, S. E. ) Ch. 10-13, 315-335 (Springer, New York, 2009).

[5] Kryukova, I. in Botanical Classification and Geographical Distribution, Apricot (ed. Smykov, V. K.) 9-23 (Agropromizdat, Moscow, 1989).

[6] Faust, M., Surányi, D. & Nyujtó, F. Origin and dissemination of apricot. Hortic. Rev. 22, 225-266 (1998).

[7] Zhebentyayeva, T. N, Ledbetter, C, Burgos, L. & Llácer, G. in Fruit Breeding, Apricot (eds Badenes, M. L. & Byrne, D. H.) 415-458 (Springer Science+Business Media: New York, 2012).

[8] Zhang, J. Y. & Zhang, Z. in Flora of Chinese Fruit Trees (eds Zhang, J. Y. & Zhang, Z. ) 42-46 (China Forestry Press: Beijing, 2003).

[9] Zhang, Q. & Liu, W. Advances of the apricot resources collection, evaluation and germplasm enhancement. Acta Hortic. Sin. 45, 1642-1660 (2018).

[10] Vavilov, N. I. The origin, variation, immunity and breeding of cultivated plants. Science 115, 433-434 (1951).

[11] Bailey, C. H. & Hough, L. F. in Advances in Fruit Breeding, Apricots. (eds Janick, J. et al. ) 367-383 (Purdue University Press, West Lafayette, Indiana, 1975).

[12] Hormaza, J., Yamane, H. & Rodrigo, J. in Genome Mapping and Molecular Breeding in Plants, Pulses, Sugar and Tuber Crops (ed Kole C.) 123-132 (Springer-Verlag Press: Berlin Heidelberg, 2007).

[13] Zohary, D., Hopf, M.. & Weiss, E. in Domestication of Plants in the Old World, third edn (eds Zohary, D., Hopf, M. & Weiss, E. ) Domestication of Plants in the Old World. 334 (Oxford University Press: Oxford, 2000).

[14] Candolle, A. D. Origin of Cultivated Plants (Appleton and Company, New York, USA, 1959).

[15] Sinskaya, E. N. Historical Geography of Cultivated Floras (at the Dawn of Agriculture) (Kolos, Leningrad, 1937).

[16] Mehlenbacher, S., Cociu, V. & Hough, L. in Genetic Resources of Temperate Fruit and Nut Crops, Apricot (Prunus) (eds Moore, J. N. & Ballington, J. R.) 63-108 (International Society for Horticultural Science, Wageningen, 1990).

[17] Gu, M. Apricot cultivars in China. Acta Hortic. 209, 63-67 (1979).

[18] Zhebentyayeva, T. N., Reighard, G. L., Gorina, V. M. & Abbott, A. G. Simple sequence repeat (SSR) analysis for assessment of genetic variability in apricot germplasm. Theor. Appl. Genet. 106, 435-444 (2003).

[19] Abbo, S. et al. Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci. 19, 351-360 (2014).

[20] Diamond, J . Evolution, consequences and future of plant and animal domestication. Nature 418, 700-707 (2002).

[21] Zhang, J. et al. Effect of domestication on the genetic diversity and structure of Saccharina japonica populations in China. Sci. Rep. 7, 42158 (2017).

[22] Chen, G. et al. Study on the main meteorological characteristics and artificial regeneration rain-collection and weeds-controlling techniques of wild fruit forest in Xinyuan. Non-wood. Res. 36, 127-135 (2018).

[23] Hipp, A. L. et al. Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. N. Phytol. 217, 439-452 (2018).

[24] Yang, X. et al. Genetic relationships among Eriobotrya species revealed by genome-wide RAD sequence data. Ecol. Evol. 7, 2861-2867 (2017).

[25] Wang, Y., Shahid, M. Q., Lin, S., Chen, C. & Hu, C. Footprints of domestication revealed by RAD-tag resequencing in loquat: SNP data reveals a non-significant domestication bottleneck and a single domestication event. BMC Genomics 18, 354 (2017).

[26] Li, M., Zhao, Z. & Miao, X. J. Genetic variability of wild apricot (Prunus armeniaca L.) populations in the Ili Valley as revealed by ISSR markers. Genet. Resour. Crop Evol. 60, 2293-2302 (2013).

[27] Yuan, Z. H. et al. Population genetic structure in apricot (Prunus armeniaca L.) cultivars revealed by fluorescent-AFLP markers in southern Xinjiang, China. J. Genet. Genomics 34, 1037-1047 (2007).

[28] Zhang, Q. P. et al. The genetic relationship and structure of some natural interspecific hybrids in Prunus subgenus Prunophora, based on nuclear and chloroplast simple sequence repeats. Genet. Resour. Crop Evol. 65, 625-636 (2017).

[29] Ren, G. et al. Genetic consequences of quaternary climatic oscillations in the Himalayas: Primula tibetica as a case study based on restriction site-associated DNA sequencing. N. Phytol. 213, 1500-1512 (2017).

[30] Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).

[31] Verde, I. et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat. Genet. 45, 487-494 (2013).

[32] Kawuki, R. S., Ferguson, M., Labuschagne, M., Herselman, L. & Kim, D.-J. Identification, characterisation and application of single nucleotide polymorphisms for diversity assessment in cassava (Manihot esculenta Crantz). Mol. Breed. 23, 669-684 (2009).

[33] Hazzouri, K. M. et al. Whole genome re-sequencing of date palms yields insights into diversification of a fruit tree crop. Nat. Commun. 6, 8824 (2015).

[34] Pereira-Dias, L., Vilanova, S., Fita, A., Prohens, J. & Rodriguez-Burruezo, A. Genetic diversity, population structure, and relationships in a collection of pepper (Capsicum spp.) landraces from the Spanish centre of diversity revealed by genotyping-by-sequencing (GBS). Hortic. Res. 6, 54 (2019).

[35] Holsinger, K. E. & Weir, B. S. Genetics in geographically structured populations: defining, estimating and interpreting F_ST . Nat. Rev. Genet. 10, 639-650 (2009).

[36] Gupta, S. K., Baek, J., Carrasquilla-Garcia, N. & Penmetsa, R. V. Genome-wide polymorphism detection in peanut using next-generation restriction-site-associated DNA (RAD) sequencing. Mol. Breed. 35, 145 (2015).

[37] Jiao, Y. et al. Genome-wide genetic changes during modern breeding of maize. Nat. Genet. 44, 812-815 (2012).

[38] Gao, Y. et al. Genetic diversity and structure of wild and cultivated Amorphophallus paeoniifolius populations in southwestern China as revealed by RAD-seq. Sci. Rep. 7, 14183 (2017).

[39] Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94 (2010).

[40] Kostina, K. F. The cultivation of apricots in Fergana Valley (in Russian). Bull. Appl. Bot. Genet. Plant Breed. 27, 153-158 (1931).

[41] Boulnois, L. Silk Road: Monks, Warriors & Merchants on the Silk Road (WW Norton & Co Inc, New York, 2004).

[42] He, T. M. et al. Using SSR markers to determine the population genetic structure of wild apricot (Prunus armeniaca L.) in the Ily Valley of West China. Genet. Resour. Crop Evol. 54, 563-572 (2007).

[43] Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 (1989).

[44] Hu, Z. et al. Population genomics of pearl millet (Pennisetum glaucum (L.) R. Br.): comparative analysis of global accessions and Senegalese landraces. BMC Genomics 16, 1048 (2015).

[45] Li, H. & Durbin, R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25, 1754-1760 (2009).

[46] Zhang, H. X., Li, H. Y. & Li, Y. X. Identifying evolutionarily significant units for conservation of the endangered Malus sieversii using genome-wide RADseq data. Nord. J. Bot. 36, e01733 (2018).

[47] Vilella, A. J. et al. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327-335 (2009).

[48] Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).

[49] Tang, H., Peng, J., Wang, P. & Risch, N. J. Estimation of individual admixture: analytical and study design considerations. Genet. Epidemiol. 28, 289-301 (2005).

[50] Zhou, Q. et al. Genome-wide SNP markers based on SLAF-seq uncover breeding traces in rapeseed (Brassica napus L.). Front. Plant Sci. 8, 648 (2017).

[51] Yang, J., Lee, S. H., Goddard, M. E. & Visscher, P. M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76-82 (2011).

[52] Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

[53] Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Commun. 8, 249 (2017).

[54] Watterson, G. A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256-276 (1975).

[55] Hudson, R. R., Slatkint, M. & Maddison, W. P. Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583-589 (1992).

[56] Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370 (1984).

[57] Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).

[58] Li, Y. et al. Genomic analyses yield markers for Identifying agronomically Important genes in potato. Mol. Plant 11, 473-484 (2018).

[59] Zhang, Q. et al. The genome of Prunus mume. Nat. Commun. 3, 1318 (2012).