Genome-wide association mapping of fruit-quality traits using genotyping-by-sequencing approach in citrus landraces, modern cultivars, and breeding lines in Japan
- 325 Downloads
Association mapping is an attractive method to identify QTLs in perennial horticultural crops such as citrus, as it does not need a designed cross between parental genotypes and can save time and labor to construct a segregating population. It usually requires more genetic markers than linkage-based QTL mapping owing to a lower degree of linkage disequilibrium (LD). However, recent advances in next-generation sequencing offer high-throughput, cost-effective methods, including genotyping-by-sequencing (GBS), for genotyping massive amounts of single nucleotide polymorphisms (SNPs). In this study, we performed a genome-wide association study (GWAS) of fruit-quality traits in citrus using SNPs obtained by GBS. We evaluated 110 citrus accessions, including landraces, modern cultivars, and breeding lines, for eight fruit-quality traits (fruit weight, fruit skin color, fruit surface texture, peelability, pulp firmness, segment firmness, sugar content, and acid content) during 2005 to 2012 (except 2007). GBS found 2309 SNPs, which we anchored to the clementine reference genome. We evaluated LD in the 110 accessions and confirmed that GBS gave enough SNPs to conduct GWAS. We identified seven QTLs, including four novel ones, comprising four significant QTLs for fruit weight and one QTL each for fruit skin color, pulp firmness, and segment firmness. These QTLs offer promise for use in citrus crossbreeding.
KeywordsCitrus breeding Fruit quality Single nucleotide polymorphism (SNP) Marker-assisted selection (MAS)
We would like to thank Y. Yamamura, H. Hira, and other staff members of agricultural field in Kuchinotsu Citrus Research Station, NARO for careful management of plant materials used in this study.
Data Archiving Statement
All relevant data are presented in the main paper and in the Supplementary Materials.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Chanock SJ, Manolio T, Boehnke M, Boerwinkle E, Hunter DJ, Thomas G, Hirschhorn JN, Abecasis G, Altshuler D, Bailey-Wilson JE, Brooks LD, Cardon LR, Daly M, Donnelly P, Fraumeni JF, Freimer NB, Gerhard DS, Gunter C, Guttmacher AE, Guyer MS, Harris EL, Hoh J, Hoover R, Kong CA, Merikangas KA, Morton CC, Palmer LJ, Phimister EG, Rice JP, Roberts J, Rotimi C, Tucker MA, Vogan KJ, Wacholder S, Wijsman EM, Winn DM, Collins FS (2007) Replicating genotype–phenotype associations. Nature 447:655–660CrossRefPubMedGoogle Scholar
- FAO (2016) FAOSTAT. http://www.fao.org/economic/ess/en/. Accessed 29 Nov 2016
- Furr JR (1969) Citrus breeding for the arid southwestern United States. In: Chapman HD (ed) Proceedings of 1st international citrus symposium, vol 1. University of California, Riverside, CA, USA, pp 191–197Google Scholar
- Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2015) ASReml user guide release 4.1. VSN International Ltd., Hemel HempsteadGoogle Scholar
- Gmitter FG, Chen C, Nagesware R, Soneji JR (2007) 14 Citrus fruits. In: Kole C (ed) Genome mapping and molecular breeding in plants, volume 4: Fruits and nuts. Springer-Verlag, Berlin Heidelberg, pp 265–279Google Scholar
- Hearn CJ, Bai J, Baldwin E, McCollum TG, Hall DG, Stover E, Driggers R (2014) Breeding “sweet oranges” at the USDA US Horticultural Research Laboratory. In XXIX International Horticultural Congress on Horticulture: sustaining lives, livelihoods and landscapes (IHC2014): 1127 (pp. 41–44)Google Scholar
- Kouassi AB, Durel CE, Costa F, Tartarini S, van de Weg E, Evans K, Fernandez-Fernandez F, Govan C, Boudichevskaja A, Dunemann F, Antofie A, Lateur M, Stankiewicz-Kosyl M, Soska A, Tomala K, Lewandowski M, Rutkovski K, Zurawicz E, Guerra W, Laurens F (2009) Estimation of genetic parameters and prediction of breeding values for apple fruit-quality traits using pedigreed plant material in Europe. Tree Genet Genomes 5:659–672CrossRefGoogle Scholar
- Minamikawa MF, Nonaka K, Kaminuma E, Kajiya-Kanegae H, Onogi A, Goto S, Yoshioka T, Imai A, Hamada H, Hayashi T, Matsumoto S, Katayose Y, Toyoda A, Fujiyama A, Nakamura Y, Shimizu T, Iwata H (2017) Genome-wide association study and genomic prediction in citrus: potential of genomics-assisted breeding for fruit quality traits. Sci Rep 7:4721CrossRefPubMedPubMedCentralGoogle Scholar
- Ollitrault P, Terol J, Chen CX, Federici CT, Lotfy S, Hippolyte I, Ollitrault F, Bérard A, Chauveau A, Cuenca J, Costantino G, Kacar Y, Mu L, Garcia-Lor A, Froelicher Y, Aleza P, Boland A, Billot C, Navarro L, Luro F, Roose ML, Gmitter FG, Talon M, Brunel D (2012) A reference genetic map of C. clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 13:593CrossRefPubMedPubMedCentralGoogle Scholar
- Oueslati A, Salhi-Hannachi A, Luro F, Vignes H, Mournet P, Ollitrault P (2017) Genotyping by sequencing reveals the interspecific C. maxima / C. reticulata admixture along the genomes of modern citrus varieties of mandarins, tangors, tangelos, orangelos and grapefruits. PLoS One 12:e0185618CrossRefPubMedPubMedCentralGoogle Scholar
- Soetaert K (2013) plot3D: plotting multi-dimensional data. R package version 1.0Google Scholar
- Soost RK (1987) Breeding citrus-genetics and nucellar embryony. Improving vegetatively propagated crops. Academic Press, London, pp 83–110Google Scholar
- Turner SD (2014) qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. bioRxiv (2014): 005165Google Scholar
- Turner S, Armstrong LL, Bradford Y, Carlson CS, Crawford DC, Crenshaw AT, de Andrade M, Doheny KF, Haines JL, Hayes G, Jarvik G, Jiang L, Kullo IJ, Li R, Ling H, Manolio TA, Matsumoto M, McCarty CA, McDavid AN, Mirel DB, Paschall JE, Pugh EW, Rasmussen LV, Wilke RA, Zuvich RL, Ritchie MD (2011) Quality control procedures for genome-wide association studies. Curr Protoc Hum Genet Chapter 1: Unit1 19Google Scholar
- Wiggans GR, Sonstegard TS, Vanraden PM, Matukumalli LK, Schnabel RD, Taylor JF, Schenkel FS, Van Tassell CP (2009) Selection of single-nucleotide polymorphisms and quality of genotypes used in genomic evaluation of dairy cattle in the United States and Canada. J Dairy Sci 92:3431–3436CrossRefPubMedGoogle Scholar
- Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J, Takita MA, Labadie K, Poulain J, Couloux A, Jabbari K, Cattonaro F, Del Fabbro C, Pinosio S, Zuccolo A, Chapman J, Grimwood J, Tadeo FR, Estornell LH, Muñoz-Sanz JV, Ibanez V, Herrero-Ortega A, Aleza P, Pérez-Pérez J, Ramón D, Brunel D, Luro F, Chen C, Farmerie WG, Desany B, Kodira C, Mohiuddin M, Harkins T, Fredrikson K, Burns P, Lomsadze A, Borodovsky M, Reforgiato G, Freitas-Astúa J, Quetier F, Navarro L, Roose M, Wincker P, Schmutz J, Morgante M, Machado MA, Talon M, Jaillon O, Ollitrault P, Gmitter F, Rokhsar D (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32:656–662CrossRefPubMedPubMedCentralGoogle Scholar