Molecular Breeding

, 37:85

Genetic structure of a QTL hotspot on chromosome 2 in sweet cherry indicates positive selection for favorable haplotypes

  • Lichun Cai
  • Roeland E. Voorrips
  • Eric van de Weg
  • Cameron Peace
  • Amy Iezzoni
Article
  • 184 Downloads

Abstract

A genomic region of particular interest for sweet cherry (Prunus avium L.) breeding is a quantitative trait locus (QTL) “hotspot” on chromosome 2. QTLs for fruit size, firmness, sweetness, and flowering time are reported to map to this region. An understanding of genetic diversity, allele sources, linkage relationships, and historical recombinations is critical to enable the combining of favorable alleles at multiple loci. The objectives of this study were to characterize, visualize, and interpret the genetic structure of this previously identified QTL hotspot within North American sweet cherry breeding germplasm, using a pedigree-based haploblocking approach. Across the 29.4 cM (6.3 Mbp) region defined by single nucleotide polymorphism (SNP) information from the RosBREED cherry 6K SNP array v1, a total of 12 recombination events falling into six inter-marker regions were traced within the pedigree of elite and wild germplasm (n = 55). These recombinations defined five haploblocks containing 5–15 markers and exhibiting 7–11 haplotypes each. Over the entire QTL hotspot, 30 extended haplotypes were identified for which parental gametes could be determined. When the haploblocks and their haplotypes were used to explore genetic diversity, ancestry, and recombination patterns, and then integrated with previous QTL results for fruit size, the results indicated that favorable alleles at this QTL hotspot are under positive selection in breeding. The genetic framework provided by a haploblock approach and knowledge of haplotype-level diversity sets the stage for assigning breeding utility to these haplotypes.

Keywords

Prunus avium Haplotype SNP QTL hotspot 

Supplementary material

11032_2017_689_MOESM1_ESM.xlsx (16 kb)
Supplementary Table S1Sweet cherry plant materials and their parentage information. (XLSX 15 kb)
11032_2017_689_MOESM2_ESM.xlsx (11 kb)
Supplementary Table S2Descriptions of locations (cM, bp) and lengths (cM, Mbp) of the haploblocks and gaps between sweet cherry haploblocks identified for a QTL hotspot on chromosome 2 in the sweet cherry breeding germplasm listed in Table S1. (XLSX 10 kb)
11032_2017_689_MOESM3_ESM.xlsx (12 kb)
Supplementary Table S3Frequencies and founder contributors of haplotypes identified for five haploblocks spanning a QTL hotspot on chromosome 2, calculated for elite and wild germplasm only. (XLSX 11 kb)
11032_2017_689_MOESM4_ESM.xlsx (15 kb)
Supplementary Table S4Haplotypes observed across five haploblocks for a QTL hotspot on chromosome 2 in U.S. elite and wild sweet cherry breeding germplasm for which parental gametes could be determined (n=55). (XLSX 14 kb)
11032_2017_689_MOESM5_ESM.docx (1 mb)
Supplementary Fig. S1(A) Recombination sites identified for determining haploblock boundaries of a QTL hotspot on chromosome 2, illustrated using the Segregation Indicator Pattern and Recombination Sequence parameters of FlexQTL™. Phased marker genotype data for a maternal parent (‘Van’) – paternal parent (‘Lapins’) – child (‘Sweetheart’) combination is shown. For each individual, alleles in the left column were inherited from the maternal parent and alleles on the right column were from the paternal parent. ‘0’ or ‘1’ indicates the grandparental origin of alleles (maternal or paternal, respectively). Recombination Sequences are marked by black line boxes. Recombination sites are highlighted by red lines. Six recombination sites used for delimiting the QTL hotspot’s five haploblocks were identified from elite germplasm including EE, ‘Sweetheart’, ‘Lapins’, and ‘Stella’. Examples of within-haploblock recombination are illustrated with five unselected offspring from different families. For example, offspring 4 was determined to have inherited a gamete with a recombination within HB-E between the SNPs located at 19,200,549 and 19,324,328. (B) Pedigree of individuals presented in Supplementary Fig. S1 (A). (DOCX 1054 kb)
11032_2017_689_MOESM6_ESM.docx (276 kb)
Supplementary Fig. S2Marker allele composition of each haplotype across five haploblocks for the sweet cherry QTL hotspot on chromosome 2. SSR alleles are recorded as fragment sizes in base pairs. The smallest subset of markers needed to differentiate the haplotypes within each haploblock are highlighted in red font. Haplotypes were assigned by the PediHaplotyper software (Voorrips et al. 2016). Haplotypes containing missing marker scores were omitted from the table. (DOCX 275 kb)

References

  1. Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel CE, Kouassi AB, Laurens F, Mathis F, Gessler C, Gobbin D, Rezzonico F, Patocchi A, Kellerhals M, Boudichevskaia A, Dunemann F, Peil A, Nowicka A, Lata B, Stankiewicz-Kosyl M, Jeziorek K, Pitera E, Soska A, Tomala K, Evans KM, Fernández-Fernández F, Guerra W, Korbin M, Keller S, Lewandowski M, Plocharski W, Rutkowski K, Zurawicz E, Costa F, Sansavini S, Tartarini S, Komjanc M, Mott D, Antofie A, Lateur M, Rondia A, Gianfranceschi L, van de Weg WE (2014) Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet 127(5):1073–1090PubMedGoogle Scholar
  2. Cabrera A, Rosyara UR, De Franceschi P, Sebolt A, Sooriyapathirana SS, Dirlewanger E, Quero-Garcia J, Schuster M, Iezzoni AF, van der Knaap E (2012) Rosaceae conserved orthologous sequences marker polymorphism in sweet cherry germplasm and construction of a SNP map. Tree Genet Genomes 8:237–247CrossRefGoogle Scholar
  3. Campoy JA, Dantec L, Barreneche T, Dirlewanger E, Guero-Garcia J (2015) New insights into fruit firmness and weight control in sweet cherry. Plant Mol Biol Rep 33(4):783–796CrossRefGoogle Scholar
  4. Campoy JA, Lerigoleur-Balsemin E, Christmann H, Beauvieux R, Girollet N, Quero-Garcia J, Dirlewanger E, Barrenecha T (2016) Genetic diversity, linkage disequilibrium, population structure and construction of a core collection of Prunus avium L. landraces and bred cultivars. BMC Plant Biol 16:49CrossRefPubMedPubMedCentralGoogle Scholar
  5. Castède S, Campoy JA, García JQ, Le Dantec L, Lafargue M, Barreneche T, Wenden B, Dirlewanger E (2014) Genetic determinism of phenological traits highly affected by climate change in Prunus avium: flowering data dissected into chilling and heat requirements. New Phytol 202(2):703–715CrossRefPubMedGoogle Scholar
  6. Choi C, Kappel F (2004) Inbreeding, coancestry, and founding clones of sweet cherries from North America. J Am Soc Hortic Sci 129:535–543Google Scholar
  7. De Franceschi P, Stegmeir T, Cabrera A, van de Knaap E, Rosyara UR, Sebolt AM, Dondini L, Dirlewanger E, Quero-Garcia J, Campoy JA, Iezzoni AF (2013) Cell number regulator genes in Prunus provide candidate genes for the control of fruit size in sweet and sour cherry. Mol Breed 32:311–326CrossRefPubMedPubMedCentralGoogle Scholar
  8. Farsad A, Esna-Ashari M (2016) Genetic diversity of some Iranian sweet cherry (Prunus avium) cultivars using microsatellite markers and morphological traits. Cytol Genet 50(1):9–19CrossRefGoogle Scholar
  9. Jaganathan D, Thudi M, Kale S, Azam S, Roorkiwal M, Gaur PM, Kishor PBK, Nguyen H, Sutton T, Varshney RK (2015) Genotyping-by-sequencing based intra-specific genetic map refinds a “QTL-hotspot” region for drought tolerance in chickpea. Mol Gen Genomics 290:559–571CrossRefGoogle Scholar
  10. Klagges C, Campoy JA, Quero-Garcia J, Guzman A, Mansur L, Gratacos E, Silva H, Rosyara UR, Iezzoni A, Meisel LA, Dirlewanger E (2013) Construction and comparative analyses of highly dense linkage maps of two sweet cherry intra-specific progenies of commercial cultivars. PLoS One 8(1):e54743CrossRefPubMedPubMedCentralGoogle Scholar
  11. Lacis G, Rashal I, Ruisa S, Trajkovski V, Iezzoni AF (2009) Assessment of genetic diversity of Latvian and Swedish sweet cherry (Prunus avium L.) genetic resources collections by using SSR (microsatellite) markers. Sci Hortic 121(4):451–457CrossRefGoogle Scholar
  12. Lane WD, MacDonald RA (1996) Sweetheart sweet cherry. Can J Plant Sci 76:161–163CrossRefGoogle Scholar
  13. 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 11:77CrossRefPubMedPubMedCentralGoogle Scholar
  14. Peace C, Bassil N, Main D, Ficklin S, Rosyara UR, Stegmeir T, Sebolt A, Gilmore B, Lawley C, Mockler TC, Bryant DW, Wilhelm L, Iezzoni A (2012) Development and evaluation of a genome-wide 6K SNP array for diploid sweet cherry and tetraploid sour cherry. PLoS One 7(12):e48305CrossRefPubMedPubMedCentralGoogle Scholar
  15. Peace C, Luby J, van de Weg WE, Bink MCAM, Iezzoni A (2014) A strategy for developing representative germplasm sets for systematic QTL validation, demonstrated for apple, peach and sweet cherry. Tree Genet Genomes 10(6):1679–1694CrossRefGoogle Scholar
  16. Rosyara U, Bink M, van de Weg WE, Zhang G, Wang D, Sebolt A, Dirlewanger E, Quero-Garcia J, Schuster M, Iezzoni A (2013) Fruit size QTL identification and the prediction of parental QTL genotypes and breeding values in multiple pedigreed populations of sweet cherry. Mol Breed 32:875–887CrossRefGoogle Scholar
  17. Sharma K, Xuan H, Sedlák P (2015) Assessment of genetic diversity of Czech sweet cherry cultivars using microsatellite markers. Biochem Syst Ecol 63:6–12CrossRefGoogle Scholar
  18. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel LA, Decroocq V, Sosinski B, Prochnik S, Mitros T, Policriti A, Cipriani G, Dondini L, Ficklin S, Goodstein DM, Xuan P, Del Fabbro C, Aramini V, Copetti D, Gonzalez S, Horner DS, Ralchi R, Lucas S, Mica E, Maldonado J, Lazzari B, Bielenberg D, Pirona R, Miculan M, Barakat A, Testolin R, Stella A, Tartarini S, Tonutti P, Arús P, Orellana A, Wells C, Main D, Vizzotto G, Silva H, Salamini F, Schmutz J, Morgante M, Rokhsar DS (2013) The high-quality draft of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494CrossRefPubMedGoogle Scholar
  19. Verde I, Jenkins J, Dondini L, Micali S, Pagliarani G, Vendramin E, Paris R, Aramini V, Gazza L, Rossini L, Bassi D, Troggio M, Shu S, Grimwood J, Tartarini S, Dettori MT, Schmutz J (2017) The peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics 18:225CrossRefPubMedPubMedCentralGoogle Scholar
  20. Voorrips RE, Bink MCAM, van de Weg WE (2012) Pedimap: software for the visualization of genetic and phenotypic data in pedigrees. J Hered 103(6):903–907CrossRefPubMedPubMedCentralGoogle Scholar
  21. Voorrips RE, Bink MCAM, Kruisselbrink JW, Koehorst-van Putten HJ, van de Weg WE (2016) PediHaplotyper: software for consistent assignment of marker haplotypes in pedigrees. Mol Breed 36:119CrossRefPubMedPubMedCentralGoogle Scholar
  22. Wünsch A, Hormaza JI (2002) Molecular characterization of sweet cherry (Prunus avium L.) genotypes using peach [Prunus persica (L.) Batsch] SSR sequences. Heredity 89:56–63CrossRefPubMedGoogle Scholar
  23. Zhang G, Sebolt A, Sooriyapathirana S, Wang D, Bink M, Olmstead J, Iezzoni A (2010) Fruit size QTL analysis of an F1 population derived from a cross between a domesticated sweet cherry cultivar and a wild forest sweet cherry. Tree Genet Genomes 6:25–36CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Lichun Cai
    • 1
  • Roeland E. Voorrips
    • 2
  • Eric van de Weg
    • 2
  • Cameron Peace
    • 3
  • Amy Iezzoni
    • 1
  1. 1.Department of HorticultureMichigan State UniversityEast LansingUSA
  2. 2.Plant BreedingWageningen University and ResearchWageningenThe Netherlands
  3. 3.Department of HorticultureWashington State UniversityPullmanUSA

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