Genomic prediction and genome-wide association study using combined genotypic data from different genotyping systems: application to apple fruit quality traits

Mai F. Minamikawa , Miyuki Kunihisa , Shigeki Moriya , Tokurou Shimizu , Minoru Inamori , Hiroyoshi Iwata

Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) : 131

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) :131 DOI: 10.1093/hr/uhae131
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Genomic prediction and genome-wide association study using combined genotypic data from different genotyping systems: application to apple fruit quality traits
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Abstract

With advances in next-generation sequencing technologies, various marker genotyping systems have been developed for genomics-based approaches such as genomic selection (GS) and genome-wide association study (GWAS). As new genotyping platforms are developed, data from different genotyping platforms must be combined. However, the potential use of combined data for GS and GWAS has not yet been clarified. In this study, the accuracy of genomic prediction (GP) and the detection power of GWAS increased for most fruit quality traits of apples when using combined data from different genotyping systems, Illumina Infinium single-nucleotide polymorphism array and genotyping by random amplicon sequencing-direct (GRAS-Di) systems. In addition, the GP model, which considered the inbreeding effect, further improved the accuracy of the seven fruit traits. Runs of homozygosity (ROH) islands overlapped with the significantly associated regions detected by the GWAS for several fruit traits. Breeders may have exploited these regions to select promising apples by breeders, increasing homozygosity. These results suggest that combining genotypic data from different genotyping platforms benefits the GS and GWAS of fruit quality traits in apples. Information on inbreeding could be beneficial for improving the accuracy of GS for fruit traits of apples; however, further analysis is required to elucidate the relationship between the fruit traits and inbreeding depression (e.g. decreased vigor).

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Mai F. Minamikawa, Miyuki Kunihisa, Shigeki Moriya, Tokurou Shimizu, Minoru Inamori, Hiroyoshi Iwata. Genomic prediction and genome-wide association study using combined genotypic data from different genotyping systems: application to apple fruit quality traits. Horticulture Research, 2024, 11 (7) : 131 DOI:10.1093/hr/uhae131

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Acknowledgements

We are grateful to all the members of the NARO Institute of Fruit Tree and Tea Science for maintaining the apple trees. This research was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics-based Technology for Agricultural Improvement, NGB-2007 and 2010), Cabinet Office, Government of Japan, Cross-ministerial Strategic Innovation Promotion Program (SIP), ‘Technologies for Smart Bio-industry and Agriculture’ (funding agency: Bio-oriented Technology Research Advancement Institution, NARO), MAFF commissioned project study on ‘Smart breeding technologies to Accelerate the development of new varieties toward achieving “Strategy for Sustainable Food Systems, MIDORI”’ Grant Number JPJ012037 and a Grant-in-Aid for JSPS Research Fellow (JP22K20577 and JP23K13928).

Author contributions

M.F.M. and M.K. conceived and designed the study. M.K. and S.M. extracted DNA and performed SNP genotyping. T.S. helped with SNP genotyping. S.M. performed the phenotyping. M.I. improved the estimation algorithm for the parental phase. M.F.M. combined the genotypes obtained using different genotyping systems and performed GP and GWAS. H.I. provided technical help for the statistical analysis. M.F.M., M.K., and S.M. drafted the manuscript. All the authors have read and approved the manuscript.

Data availability

Information on DNA markers is available from Supplementary Data Tables.

Conflict of interest statement

None declared.

Competing financial interests

The authors declare no competing financial interests.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Iwata H, Minamikawa MF, Kajiya-Kanegae H. et al. Genomics-assisted breeding in fruit trees. Breed Sci. 2016; 66:100-15

[2]

Wang R, Li X, Sun M. et al. Genomic insights into domestication and genetic improvement of fruit crops. Plant Physiol. 2023; 192:2604-27

[3]

Jannink JL, Lorenz AJ, Iwata H. Genomic selection in plant breeding: from theory to practice. Brief Funct Genomics. 2010; 9:166-77

[4]

Lorenz AJ, Chao S, Asoro FG. et al. Genomic Selection In Plant Breeding: Knowledge and Prospects. Adv Agron. 2011; 110:77-123

[5]

Khan MA, Korban SS. Association mapping in forest trees and fruit crops. J Exp Bot. 2012; 63:4045-60

[6]

Heffner EL, Lorenz AJ, Jannink JL. et al. Plant breeding with genomic selection: gain per unit time and cost. Crop Sci. 2010; 50:1681-90

[7]

Bianco L, Cestaro A, Linsmith G. et al. Development and validation of the Axiom® Apple480K SNP genotyping array. Plant J. 2016; 86:62-74

[8]

Koning-Boucoiran CFS, Danny Esselink G, Vukosavijev M. et al. Using RNA-seq to assemble a rose transcriptome with more than 13,000 full-length expressed genes and to develop the WagRhSNP 68k Axiom SNP array for rose (Rosa L.). Front Plant Sci. 2015; 6:1-10

[9]

Chagné D, Crowhurst RN, Troggio M. et al. Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One. 2012; 7:e31745

[10]

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

[11]

Elshire RJ, Glaubitz JC, Sun Q. et al.A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011; 6:1-10

[12]

Baird NA, Etter PD, Atwood TS. et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008; 3:1-7

[13]

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

[14]

Li J, Zhang M, Li X. et al. Pear genetics: recent advances, new prospects, and a roadmap for the future. Hortic Res. 2022; 9:9

[15]

Enoki H, Takeuchi Y.New genotyping technology, GRAS-Di, using next generation sequencer. Proceedings of Plant and Animal Genome Conference XXVI. 2018

[16]

Howard NP, Troggio M, Durel CE. 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; 22:1-18

[17]

Minamikawa MF, Kunihisa M, Noshita K. et al. Tracing founder haplotypes of Japanese apple varieties: application in genomic prediction and genome-wide association study. Hortic Res. 2021; 8:49

[18]

Noiton DAM, Alspach PA. Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci. 1996; 121:773-82

[19]

Janick J, Moore JN. ( Tropical Fruits. ( Vol 1).Eds.) Fruit Breeding, Tree and John Wiley & Sons: NJ, USA, 1996

[20]

Onoue N, Kono A, Azuma A. et al. Inbreeding depression in yield-related traits revealed by high-throughput sequencing in hexaploid persimmon breeding populations. Euphytica. 2022; 218:1-18

[21]

Imai A, Nonaka K, Kuniga T. et al. Genome-wide association mapping of fruit-quality traits using genotyping-by-sequencing approach in citrus landraces, modern cultivars, and breeding lines in Japan. Tree Genet Genomes. 2018; 14:24

[22]

Xiang T, Christensen OF, Vitezica ZG. et al. Genomic evaluation by including dominance effects and inbreeding depression for purebred and crossbred performance with an application in pigs. Genet Sel Evol. 2016; 48:1-14

[23]

Moriya S, Kunihisa M, Okada K. et al. Identification of QTLs for flesh mealiness in apple (Malus × domestica Borkh.). Hortic J. 2017; 86:159-70

[24]

Kunihisa M, Moriya S, Abe K. et al. Identification of QTLs for fruit quality traits in Japanese apples: QTLs for early ripening are tightly related to preharvest fruit drop. Breed Sci. 2014; 64:240-51

[25]

Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007; 81:1084-97

[26]

VanRaden PM, O’Connell JR, Wiggans GR. et al. Genomic evaluations with many more genotypes. Genet Sel Evol. 2011; 43:10

[27]

Li Y, Willer CJ, Ding J. et al. MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet Epidemiol. 2010; 34:816-34

[28]

Scheet P, Stephens M. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet. 2006; 78:629-44

[29]

Mikhchi A, Honarvar M, Kashan NEJ. et al. Assessing and comparison of different machine learning methods in parent-offspring trios for genotype imputation. J Theor Biol. 2016; 399:148-58

[30]

Yang Y, Wang Q, Chen Q. et al. A new genotype imputation method with tolerance to high missing rate and rare variants. PLoS One. 2014; 9:9

[31]

Jattawa D, Elzo MA, Koonawootrittriron S. et al. Imputation accuracy from low to moderate density single nucleotide polymorphism chips in a Thai multibreed dairy cattle population. Asian Australas J Anim Sci. 2016; 29:464-70

[32]

Desta ZA, Ortiz R. Genomic selection: genome-wide prediction in plant improvement. Trends Plant Sci. 2014; 19:592-601

[33]

Korte A, Farlow A. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods. 2013; 9:29

[34]

Muqaddasi QH, Zhao Y, Rodemann B. et al. Genome-wide association mapping and prediction of adult stage Septoria tritici blotch infection in European winter wheat via high-density marker arrays. Plant Genome. 2019; 12:180029

[35]

Jung M, Roth M, Aranzana MJ. et al. The apple REFPOP—a reference population for genomics-assisted breeding in apple. Hortic Res. 2020; 7:189

[36]

Wood AR, Esko T, Yang J. et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014; 46:1173-86

[37]

Hamblin MT, Jannink J-L. Factors affecting the power of haplotype markers in association studies. Plant Genome. 2011; 4:145-53

[38]

Ru S, Main D, Evans K. et al. Current applications, challenges, and perspectives of marker-assisted seedling selection in Rosaceae tree fruit breeding. Tree Genet Genomes. 2015; 11:1-12

[39]

Aprea E, Charles M, Endrizzi I. et al. Sweet taste in apple: the role of sorbitol, individual sugars, organic acids and volatile compounds. Sci Rep. 2017; 7:1-10

[40]

Korban SS. ( Ed.) The Apple Genome. Springer: Berlin Heidelberg, Germany, 2021

[41]

Verma S, Evans K, Guan Y. et al. Two large-effect QTLs, Ma and Ma3, determine genetic potential for acidity in apple fruit: breeding insights from a multi-family study. Tree Genet Genomes. 2019; 15:1-17

[42]

Bai Y, Dougherty L, Li M. et al. A natural mutation-led truncation in one of the two aluminum-activated malate transporter-like genes at the Ma locus is associated with low fruit acidity in apple. Mol Gen Genomics. 2012; 287:663-78

[43]

Khan SA, Beekwilder J, Schaart JG. et al. Differences in acidity of apples are probably mainly caused by a malic acid transporter gene on LG16. Tree Genet Genomes. 2013; 9:475-87

[44]

Li C, Dougherty L, Coluccio AE. et al. Apple ALMT9 requires a conserved C-terminal domain for malate transport underlying fruit acidity. Plant Physiol. 2020; 182:992-1006

[45]

Sun R, Chang Y, Yang F. et al. A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality. BMC Genomics. 2015; 16:1-15

[46]

Jia D, Shen F, Wang Y. et al. Apple fruit acidity is genetically diversified by natural variations in three hierarchical epistatic genes: MdSAUR37, MdPP2CH and MdALMTII. Plant J. 2018; 95:427-43

[47]

Harker FR, Marsh KB, Young H. et al. Sensory interpretation of instrumental measurements 2: sweet and acid taste of apple fruit. Postharvest Biol Technol. 2002; 24:241-50

[48]

Kouassi AB, Durel CE, Costa F. et al. Estimation of genetic parameters and prediction of breeding values for apple fruit-quality traits using pedigreed plant material in Europe. Tree Genet Genomes. 2009; 5:659-72

[49]

Liu W, Chen Z, Jiang S. et al. Research progress on genetic basis of fruit quality traits in apple (Malus × domestica). Front Plant Sci. 2022; 13:1-11

[50]

Wang Z, Ma B, Yang N. et al. Variation in the promoter of the sorbitol dehydrogenase gene MdSDH2 affects binding of the transcription factor MdABI3 and alters fructose content in apple fruit. Plant J. 2022; 109:1183-98

[51]

Liao L, Zhang W, Zhang B. et al. Unraveling a genetic roadmap for improved taste in the domesticated apple. Mol Plant. 2021; 14:1454-71

[52]

Ablondi M, Sabbioni A, Stocco G. et al. Genetic diversity in the Italian Holstein dairy cattle based on pedigree and SNP data prior and after genomic selection. Front Vet Sci. 2022; 8:1-11

[53]

Amyotte B, Bowen AJ, Banks T. et al. Mapping the sensory perception of apple using descriptive sensory evaluation in a genome wide association study. PLoS One. 2017; 12:1-25

[54]

Urrestarazu J, Muranty H, Denancé C. et al. Genome-wide association mapping of flowering and ripening periods in apple. Front Plant Sci. 2017; 8:1-19

[55]

Jiang L, Geng D, Zhi F. et al. A genome-wide association study provides insights into fatty acid synthesis and metabolism in Malus fruits. J Exp Bot. 2022; 73:7467-76

[56]

Kumar S, Deng CH, Hunt M. et al. Homozygosity mapping reveals population history and trait architecture in self-incompatible pear (Pyrus spp.). Front Plant Sci. 2021; 11:1-12

[57]

Darwin C. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray: London, UK, 1859

[58]

Hayes B, Goddard M. Genome-wide association and genomic selection in animal breeding. Genome. 2010; 53:876-83

[59]

Moriya S, Kunihisa M, Okada K. et al. Allelic composition of MdMYB1 drives red skin color intensity in apple (Malus × domestica Borkh.) and its application to breeding. Euphytica. 2017; 213:78

[60]

Daccord N, Celton JM, Linsmith G. et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017; 49:1099-106

[61]

Hosoya S, Hirase S, Kikuchi K. et al. Random PCR-based genotyping by sequencing technology GRAS-Di (genotyping by random amplicon sequencing, direct) reveals genetic structure of mangrove fishes. Mol Ecol Resour. 2019; 19:1153-63

[62]

Li H.Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at arXiv. 2013

[63]

Li H, Handsaker B, Wysoker A. et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25:2078-9

[64]

Depristo MA, Banks E, Poplin R. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011; 43:491-8

[65]

Danecek P, Auton A, Abecasis G. et al. The variant call format and VCFtools. Bioinformatics. 2011; 27:2156-8

[66]

Browning BL, Zhou Y, Browning SR. A one-penny imputed genome from next-generation reference panels. Am J Hum Genet. 2018; 103:338-48

[67]

Browning BL, Tian X, Zhou Y. et al. Fast two-stage phasing of large-scale sequence data. Am J Hum Genet. 2021; 108:1880-90

[68]

Hamazaki K, Iwata H. Rainbow: haplotype-based genome-wide association study using a novel SNP-set method. PLoS Comput Biol. 2020; 16:e1007663

[69]

Wellmann R. Optimum contribution selection for animal breeding and conservation: the R package optiSel. BMC Bioinformatics. 2019; 20:1-13

[70]

Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer: Berlin Heidelberg, Germany, 2009

[71]

Jung S, Lee T, Cheng CH. et al.15 years of GDR: new data and functionality in the genome database for Rosaceae. Nucleic Acids Res. 2019;47:D1137-45

[72]

Endelman JB. Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome. 2011; 4:250-5

[73]

Minamikawa MF, Nonaka K, Kaminuma E. et al. Genome-wide association study and genomic prediction in citrus: potential of genomics-assisted breeding for fruit quality traits. Sci Rep. 2017; 7:4721

[74]

Biscarini F, Cozzi P, Gaspa G. et al. detectRUNS: detect runs of homozygosity and runs of heterozygosity in diploid genomes. R package version 0.9.6. 2019, May 2024, date last accessed)

[75]

Fabbri MC, Dadousis C, Tiezzi F. et al. Genetic diversity and population history of eight Italian beef cattle breeds using measures of autozygosity. PLoS One. 2021; 16:1-21

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