A new method to reconstruct the direction of parent-offspring duo relationships using SNP array data and its demonstration on ancient and modern cultivars in the outcrossing species Malus × domestica

Abstract

Unordered parent-offspring (PO) relationships are an outstanding issue in pedigree reconstruction studies. Resolution of the order of these relationships would expand the results, conclusions, and usefulness of such studies; however, no such PO order resolution (POR) tests currently exist. This study describes two such tests, demonstrated using SNP array data in the outcrossing species apple (Malus × domestica) on a PO relationship of known order (‘Keepsake’ as a parent of ‘Honeycrisp’) and two PO relationships previously ordered only via provenance information. The first test, POR-1, tests whether some of the extended haplotypes deduced from homozygous SNP calls from one individual in an unordered PO duo are composed of recombinant haplotypes from accurately phased SNP genotypes from the second individual. If so, the first individual would be the offspring of the second individual, otherwise the opposite relationship would be present. The second test, POR-2, does not require phased SNP genotypes and uses similar logic as the POR-1 test, albeit in a different approach. The POR-1 and POR-2 tests determined the correct relationship between ‘Keepsake’ and ‘Honeycrisp’. The POR-2 test confirmed ‘Reinette Franche’ as a parent of ‘Nonpareil’ and ‘Brabant Bellefleur’ as a parent of ‘Court Pendu Plat’. The latter finding conflicted with the recorded provenance information, demonstrating the need for these tests. The successful demonstration of these tests suggests they can add insights to future pedigree reconstruction studies, though caveats, like extreme inbreeding or selfing, would need to be considered where relevant.

References

[1] Evans KM, Patocchi A, Rezzonico F et al. Genotyping of pedigreed apple breeding material with a genome-covering set of SSRs: trueness-to-type of cultivars and their parentages. Mol Breed. 2011; 28: 535-47.

[2] Rosyara UR, Sebolt AM, Peace C et al. Identification of the paternal parent of ‘Bing’ sweet cherry and confirmation of descendants using single nucleotide polymorphism markers. J Am Soc Hortic Sci. 2014; 139: 148-56.

[3] Howard NP, van de Weg E, Bedford DS et al. Elucidation of the ‘Honeycrisp’ pedigree through haplotype analysis with a multi-family integrated SNP linkage map and a large apple (Malus × domestica) pedigree-connected SNP data set. Hortic Res. 2017; 4: 1-7.

[4] van de Weg E, Di Guardo M, Jänsch M et al. Epistatic fire blight resistance QTL alleles in the apple cultivar ‘Enterprise’ and selection X-6398 discovered and characterized through pedigree-informed analysis. Mol Breed. 2017; 38: 5.

[5] Larsen B, Gardner K, Pedersen C et al. Population structure, relatedness and ploidy levels in an apple gene bank revealed through genotyping-by-sequencing. PLoS One. 2018; 13: e0201889.

[6] Laucou V, Launay A, Bacilieri R et al. Extended diversity analysis of cultivated grapevine Vitis vinifera with 10K genome-wide SNPs. PLoS One. 2018; 13: e0192540.

[7] Muranty H, Denancé C, Feugey L et al. Using whole-genome SNP data to reconstruct a large multi-generation pedigree in apple germplasm. BMC Plant Biol. 2020; 20: 2.

[8] Montanari S, Postman J, Bassil NV et al. Reconstruction of the largest pedigree network for pear cultivars and evaluation of the genetic diversity of the USDA-ARS National Pyrus Collection. G3 Genes Genomes Genet. 2020; 10: 3285-97.

[9] Migicovsky Z, Gardner KM, Richards C et al. Genomic consequences of apple improvement. Hortic. Res. 2021; 8: 1-13.

[10] Di Pierro EA, Gianfranceschi L, Di Guardo M et al. A high-density, multi-parental SNP genetic map on apple validates a new mapping approach for outcrossing species. Hortic. Res. 2016; 3: 1-13.

[11] Vanderzande S, Howard NP, Cai L et al. High-quality, genome-wide SNP genotypic data for pedigreed germplasm of the diploid outbreeding species apple, peach, and sweet cherry through a common workflow. PLoS One. 2019; 14: e0210928.

[12] Cooper GM . Heredity, Genes, and DNA. In: The Cell: A Molecular Approach.2nd ed. Sunderland, MA, USA: Sinauer Associates, 2000.

[13] Howard NP, Albach DC, Luby JJ . The identification of apple pedigree information on a large diverse set of apple germplasm and its application in apple breeding using new genetic tools. In: 18th International Conference on Organic Fruit-Growing: Proceedings of the Conference.Weinsberg, Germany: Foerdergemeinschaft Oekologischer Obstbau e. V. (FOEKO), 2018.

[14] Xu K, Wang A, Brown S . Genetic characterization of the ma locus with pH and titratable acidity in apple. Mol Breed. 2012; 30: 899-912.

[15] King GJ, Lynn JR, Dover CJ et al. Resolution of quantitative trait loci for mechanical measures accounting for genetic variation in fruit texture of apple (Malus pumila mill.). Theor Appl Genet. 2001; 102: 1227-35.

[16] Kumar S, Garrick DJ, Bink MC et al. Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics. 2013; 14: 393.

[17] Buti M, Poles L, Caset D et al. Identification and validation of a QTL influencing bitter pit symptoms in apple (Malus × domestica). Mol Breed. 2015; 35: 29.

[18] Chagné D, Vanderzande S, Kirk C et al. Validation of SNP markers for fruit quality and disease resistance loci in apple (Malus × domestica Borkh.) using the OpenArray^® platform . Hortic Res. 2019; 6: 1-16.

[19] Cai L, Voorrips RE, van de Weg E et al. Genetic structure of a QTL hotspot on chromosome 2 in sweet cherry indicates positive selection for favorable haplotypes. Mol Breed. 2017; 37: 85.

[20] Jaillon O, Aury J-M, Noel B et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449: 463-7.

[21] Leroy A. Dictionnaire de Pomologie: Contenant l’histoire, la Description, la Figure Des Fruits Anciens et Des Fruits Modernes les plus généralement Connus et cultivés. Belleuvre et Dolbeau: Imprimerie Lachèse; 1873.

[22] Smith MWG . National Apple Register of the United Kingdom. London: Ministry of Agriculture, Fisheries and Food, 1971.

[23] Bianco L, Cestaro A, Sargent DJ et al. Development and validation of a 20K single nucleotide polymorphism (SNP) whole genome genotyping Array for apple (Malus × domestica Borkh). PLoS One. 2014; 9: e110377.

[24] Howard NP, Troggio M, Durel C-E et al. Integration of Infinium and axiom SNP array data in the outcrossing species Malus × domestica and causes for seemingly incompatible calls. BMC Genomics. 2021; 22: 246.

[25] Bink MCAM, Jansen J, Madduri M et al. Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet. 2014; 127: 1073-90.

[26] Voorrips RE, Bink MCAM, Kruisselbrink JW et al. PediHaplotyper: software for consistent assignment of marker haplotypes in pedigrees. Mol Breed. 2016; 36: 119.