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Association analysis for oxalate concentration in spinach

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Abstract

Reducing oxalate content of spinach is a major breeding objective. The aim of this research was to conduct association analysis and identify SNP markers associated with oxalate concentration in spinach germplasm. A total of 310 spinach genotypes, including 300 USDA germplasm accessions and ten commercial cultivars, were used for the association analysis of oxalate concentration. Genotyping by sequencing was used to identify 841 SNPs among the genotypes examined for the association analysis. The distribution of oxalate concentration showed a near normal distribution with a wide range in concentrations from 647.2 to 1286.9 mg/100 g on a fresh weight basis and 53.4 to 108.8 mg/g on a dry weight basis. The range in oxalate concentration in spinach suggests that it is a complex quantitative trait which may be controlled by multiple genes, each with a minor effect among the tested spinach panel. Association analysis indicated that six SNP markers (AYZV02031464_116, AYZV02031464_117, AYZV02031464_95, AYZV02283363_2707, AYZV02287123_2830, and AYZV02296293_852) were associated with the oxalate concentration. The SNP markers may be useful for breeders to select germplasm for reduced oxalate concentrations in spinach breeding programs through marker-assisted selection.

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References

  • Bohn T, Davidsson L, Walczyk T, Hurrell RF (2004) Fractional magnesium absorption is significantly lower in human subjects from a meal served with an oxalate-rich vegetable, spinach, as compared with a meal served with kale, a vegetable with a low oxalate content. Br J Nutr 91:601–606

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Chan-Navarrete R, Dolstra O, van Kaauwen M, van Bueren ETL, van der Linden CG (2016) Genetic map construction and QTL analysis of nitrogen use efficiency in spinach (Spinacia oleracea L). Euphytica 208:621–636

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos. Trans. R. Soc. B12(363):557–572

    Article  Google Scholar 

  • Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196

    Article  CAS  Google Scholar 

  • Correll JC, Bluhm BH, Feng C, Lamour K, du Toit LJ, Koike ST (2011) Spinach: better management of downy mildew and white rust through genomics. Eur J Plant Pathol 129:193–205

    Article  Google Scholar 

  • Dicoteau DR (2000) Vegetable crops. Printice Hall, New Jersey

    Google Scholar 

  • Dohm JC, Minoche AE, Holtgräwe D, Capella-Gutierrez S, Zakrzewski F, Tafer H, Rupp O, Sörensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldon T, Lehrach H, Weisshaar B, Himmelbauer H (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6(5):19379

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427

    Article  CAS  Google Scholar 

  • He J, Zhao X, Laroche X, Lu Z, Liu H, Li Z (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmes RP, Kennedy M (2000) Estimation of the oxalate content of foods and daily oxalate intake. Kidney Int 57:1662–1667

    Article  CAS  PubMed  Google Scholar 

  • Iquira E, Humira S, Francois B (2015) Association mapping of QTLs for Sclerotinia stem rot resistance in a collection of soybean plant introductions using a genotyping by sequencing (GBS) approach. BMC Plant Biol 15:5. doi:10.1186/s12870-014-0408-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaminishi A, Kita V (2006) Seasonal change of nitrate and oxalate concentration in relation to the growth rate of spinach cultivars. HortSceince 41:1589–1595

    CAS  Google Scholar 

  • Kawazu Y, Okimura M, Ishii T, Yui S (2003) Varietal and seasonal differences in oxalate content of spinach. Sci Hortic 97:203–210

    Article  CAS  Google Scholar 

  • Khattak J, Torp AM, Andersen SB (2006) A genetic linkage map of Spinacia oleracea and localization of a sex determination locus. Euphytica 148:311–318

    Article  CAS  Google Scholar 

  • Kisha T, Sneller CH, Diers BW (1997) Relationship between genetic distance among parents and genetic variance in populations of soybean. Crop Sci 37:1317–1325

    Article  Google Scholar 

  • Kitchen JW, Burns EE, Perry BA (1964) Calcium oxalate content of spinach (Spinacia oleracea L). Proc Am Soc Hortic Sci 84:441–445

    CAS  Google Scholar 

  • Koh E, Charoenprasert S, Mitchell AE (2012) Effect of organic and conventional cropping systems on ascorbic acid, vitamin C, flavonoids, nitrate, and oxalate in 27 varieties of spinach (Spinacia oleracea L). J Agric Food Chem 60:3144–3150

    Article  CAS  PubMed  Google Scholar 

  • Kohman EF (1939) Oxalic acid in foods and its behavior and fate in diet. J Nutr 18:233–246

    CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lester GE, Makus DJ, Hodges DM, Jifon JL (2013) Summer (Subarctic) versus winter (Subtropic) production affects spinach (Spinacia oleracea L) Leaf bionutrients: vitamins (C, E, Folate, K1, provitamin A), lutein, phenolics, and antioxidants. J Agric Food Chem 61:7019–7027

    Article  CAS  PubMed  Google Scholar 

  • Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Yu C, Li Y, Lam T, Yiu S, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Bayer M, Druka A, Russell JR, Hackett CA, Poland J, Ramsay L, Hedley PE, Waugh R (2014) An evaluation of genotyping by sequencing (GBS) to map the Breviaristatum-e (ari-e) locus in cultivated barley. BMC Genom 15:104

    Article  Google Scholar 

  • Lv J, Qi J, Shi Q, Shen D, Zhang S, Zhang A, Shao G, Li H, Sun Z, Weng Y, Shang Y, Gu X, Li X, Zhu X, Zhang J, van Treuren R, van Dooijeweert W, Zhang Z, Huang S (2012) Genetic diversity and population STRUCTURE of cucumber (Cucumis sativus L). PLoS ONE 7:46919

    Article  Google Scholar 

  • Massey LK, Roman-Smith H, Sutton RAL (1993) Effect of dietary oxalate and calcium on urinary oxalate and risk of formation of calcium oxalate kidney stones. J Am Diet Assoc 93:901–906

    Article  CAS  PubMed  Google Scholar 

  • Minoche AE, Dohm JC, Schneider J, Holtgrawe D, Viehover P, Montfort M, Sorensen TR, Weisshaar B, Himmelbauer H (2015) Exploiting single-molecule transcript sequencing for eukaryotic gene prediction. Genome Biol 16:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Moir KW (1953) The determination of oxalic acid in plants. Qld J Agric Sci 10:1–3

    CAS  Google Scholar 

  • Morelock TE, Correll JC (2008) Spinach. In: Prohens J, Nuez F (eds) Vegetables I: asteraceae, brassicaceae, chenopodiaceae, and cucurbitaceae. Springer, New York, pp 189–218

    Chapter  Google Scholar 

  • Mou B (2008) Evaluation of oxalate concentration in the US spinach germplasm collection. HortScience 43:1690–1693

    Google Scholar 

  • Murakami K, Edamoto M, Hata N, Itami Y, Masuda M (2009) Low-oxalate spinach mutant induced by chemical mutagenesis. J Jpn Soc Hortic Sci 78:180–184

    Article  CAS  Google Scholar 

  • Nimmakayala P, Levi A, Abburi L, Abburi VL, Tomason YR, Saminathan T, Vajja VG, Malkaram S, Reddy R, Wehner TC, Mitchell SE (1011) Reddy UK (2014) Single nucleotide polymorphisms generated by genotyping by sequencing to characterize genome-wide diversity, linkage disequilibrium, and selective sweeps in cultivated watermelon. BMC Genom 15:767. doi:10.1186/1471-2164-15-767

    Article  Google Scholar 

  • Noonan SC, Savage GP (1999) Oxalate content of foods and its effect on humans. Asia Pac J Clin Nutr 8:64–74

    Article  CAS  PubMed  Google Scholar 

  • Oguchi Y, Weerakkody WAP, Tanaka A, Nakazawa S, Ando T (1996) Varietal differences of quality-related compounds in leaves and petioles of spinach grown at two locations. Bull. Hiroshima Prefect Agric. Res. Cent. 64:1–9

    Google Scholar 

  • Oke OL (1969) Oxalic acid and plants and in nutrition. World Rev Nutr Diet 10:262–303

    Article  CAS  PubMed  Google Scholar 

  • Okutani I, Sugiyama N (1994) Relationship between oxalate concentration and leaf position in various spinach cultivars. HortScience 29:1019–1021

    CAS  Google Scholar 

  • Palaniswamy UR, Bible BB, McAvoy RJ (2004) Oxalic acid concentrations in purslane (Portulaca oleraceae L.) is altered by the stage of harvest and the nitrate to ammonium ratios in hydroponics. Sci. Hort. 102:267–275

    Article  CAS  Google Scholar 

  • Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi A, Buckley B, Mou B, Motes D, Morris JB, Ma J, Xiong H, Qin J, Yang W, Chitwood J, Weng Y, Lu W (2016) Association analysis of cowpea bacterial blight resistance in USDA cowpea germplasm. Euphytica 208:143–155

    Article  CAS  Google Scholar 

  • Shin J, Lee C (2015) A mixed model reduces spurious genetic associations produced by population stratification in genome-wide association studies. Genomics 105:191–196

    Article  CAS  PubMed  Google Scholar 

  • Solberg SO, Yndgaard F, Axelsson J (2015) Nitrate and oxalate in germplasm collections of spinach and other leafy vegetables. Emirates J Food Agric 27(434):698–705

    Google Scholar 

  • Sonah H, Bastien M, Iquira E, Tardivel A, Legare G (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS ONE 8:54603

    Article  Google Scholar 

  • Sonah H, O’Donoughue L, Cober E, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13(2):211–221

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Ailipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Deynze A (2014) A de novo draft assembly of spinach using Pacific Biosciences technology. Plant & Animal Genomics XXII Conference, January 10-15, 2014, San Diego, CA (http://aa314.gondor.co/webinar/a-de-novo-draft-assembly-of-spinach-using-pacific-biosciences-technology/, accessed on May 3, 2016)

  • van Deynze A, Ashrafi H, Hickey L, Peluso P, Rank D, Chin J, Rapicavoli N, Drake J, Garvin T, Schatz M (2015) Using spinach to compare technologies for whole genome assemblies. Plant & Animal Genomics XXIII Conference, January 10-14, 2015, San Diego, CA

  • Wei Z, Zhang G, Du Q, Zhang J, Li B, Zhang D (2014) Association mapping for morphological and physiological traits in Populus simonii. BMC Genet 15(Suppl 1):S3

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Crouch JH (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48:391–407

    Article  Google Scholar 

  • Xu J, Ranc N, Munos S, Rolland S, Bouchet JP, Desplat N, Le Paslier MC, Liang Y, Brunel D, Causse M (2013) Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor Appl Genet 126(3):567–581

    Article  PubMed  Google Scholar 

  • Yang J, Zaitlen NA, Goddard ME, Visscher PM, Price AL (2014) Advantages and pitfalls in the application of mixed-model association methods. Nat Genet 46:100–106

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DK, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. The Plant Genome 1:5–20

    Article  CAS  Google Scholar 

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Acknowledgments

This work is supported, in part, by the USDA National Institute of Food and Agriculture Hatch project accession number 1002423.

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Authors and Affiliations

  1. Department of Horticulture, University of Arkansas, Fayetteville, AR, 72701, USA

    Ainong Shi

  2. Crop Improvement and Protection Research Unit, USDA-ARS, 1636 E. Alisal Street, Salinas, CA, 93905, USA

    Beiquan Mou

  3. Department of Plant Pathology, University of Arkansas, Fayetteville, AR, 72701, USA

    James C. Correll

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  1. Ainong Shi
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  2. Beiquan Mou
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Correspondence to Ainong Shi, Beiquan Mou or James C. Correll.

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Shi, A., Mou, B. & Correll, J. Association analysis for oxalate concentration in spinach. Euphytica 212, 17–28 (2016). https://doi.org/10.1007/s10681-016-1740-0

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