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Inheritance of seed phytate and phosphorus levels in common bean (Phaseolus vulgaris L.) and association with newly-mapped candidate genes

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Abstract

Common bean (Phaseolus vulgaris L.) is an important, high-quality staple food that provides large amounts of protein and mineral micronutrients to the diets of people in many countries. Phytates are a storage form of organic phosphorus which is used by the plant in various stages of growth and development but can have certain anti-nutrient properties due to chelation of minerals such as iron and zinc. At the same time, phytates provide certain health benefits and therefore are the subject of both mutagenesis and breeding programs for functional foods. The objective of this study was to evaluate the quantitative trait loci (QTL) associated with seed phytate and seed phosphorus concentration and content on a per-seed basis and to develop functional molecular markers for genes from the phytic acid synthesis pathway. We used a well-characterized mapping population, DOR364 × G19833, in three field experiments with three repetitions each and two levels of soil phosphorus fertilization, as well as a large set of previously and newly developed primer pairs for the genes myo-inositol (3)P1 synthase, myo-inositol kinase and various inositol kinases. We identified an association of phytate concentration QTL with one of two paralogs of the myo-inositol (3)P1 synthase gene family, located on linkage group b01 and expressed in common bean seed rather than in vegetative tissues. We also identified QTL for phytate concentration on linkage group b06 and phytate content on linkage groups b03, b04 and b10. We provide a synteny analysis based on common bean versus soybean genome comparisons of all the phytic acid pathway genes that were genetically mapped and indicate flanking markers that can be used for marker-assisted selection when the genes themselves are not polymorphic as PCR amplicons. We can conclude that natural variability in phytate levels is controlled by the seed-expressed myo-inositol (3)P1 synthase gene (MIPS) as well as other loci in the common bean genome. This means that breeding of phytate levels in common bean must take into account allele variability at certain candidate genes, such as this seed MIPS gene, a recently cloned ABC trasnporter and additional QTL for the trait, which underlie the oligogenic inheritance for phytate concentration in common bean.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Ariza-Nieto M, Blair MW, Welch RM, Glahn RP (2007) Screening of bioavailability patterns in eight bean (Phaseolus vulgaris L.) genotypes using the Caco-2 cell in vitro model. J Agric Food Chem 55:7950–7956

    Article  PubMed  CAS  Google Scholar 

  • Blair MW, Pedraza F, Buendia H, Gaitan E, Beebe S, Gepts P, Tohme J (2003) Development of a genome wide anchored microsatellite for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374

    Article  PubMed  CAS  Google Scholar 

  • Blair MW, Astudillo C, Grusak M, Graham R, Beebe S (2009a) Inheritance of seed iron and zinc content in common bean (Phaseolus vulgaris L.). Mol Breed 23:197–207

    Article  CAS  Google Scholar 

  • Blair MW, Sandoval TA, Caldas GV, Beebe SE, Páez MI (2009b) Quantitative trait locus analysis of seed phosphorus and seed phytate content in a recombinant inbred line population of common bean (Phaseolus vulgaris L.). Crop Sci 49:237–246

    Article  CAS  Google Scholar 

  • Blair MW, Medina JI, Astudillo C, Rengifo J, Beebe SE, Machado G, Graham R (2010) QTL for seed iron and zinc concentrations in a recombinant inbred line population of Mesoamerican common beans (Phaseolus vulgaris L.). Theor Appl Genet 121:1059–1071

    Google Scholar 

  • Bouis HE (2003) Micronutrient fortification of plants through plant breeding: can it improve nutrition in man at low cost? Proc Nutr Soc 62:403–411

    Article  PubMed  Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

  • Campion B, Sparvoli F, Doria E, Tagliabue G, Galasso I, Fileppi M, Bollini R, Nielsen E (2009) Isolation and characterisation of an lpa (low phytic acid) mutant in common bean (Phaseolus vulgaris L.). Theor Appl Genet 118:1211–1221

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cichy K, Raboy V (2009) Evaluation and development of low-phytate crops. In: Modification of seed composition to promote health and nutrition. ASSA-CSSA Publications, Monograph 51, pp 177–200

  • Cichy KA, Forster S, Grafton KF, Hosfield GL (2005) Inheritance of seed zinc accumulation in navy bean. Crop Sci 45:864–870

    Article  CAS  Google Scholar 

  • Cichy KA, Caldas GV, Snapp SS, Blair MW (2009) QTL analysis of seed iron, zinc, and phosphorus levels in an Andean bean population. Crop Sci 49:1742–1750

    Article  CAS  Google Scholar 

  • Coelho CMM, Santos JCP, Tsai SM, Vitorello VA (2002) Seed phytate content and phosphorus uptake and distribution in dry bean genotypes. Braz J Plant Physiol 14:51–58

    Article  CAS  Google Scholar 

  • Fileppi M, Galasso I, Tagliabue G, Daminati MG, Campion B, Doria E, Sparvoli F (2009) Characterization of structural genes involved in phytic acid biosynthesis in common bean (Phaseolus vulgaris L.). Mol Breed 25:453–470

    Article  Google Scholar 

  • Frossard E, Bucher M, Machler F, Mozafar A, Hurrell R (2000) Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J Sci Food Agric 80:861–879

    Article  CAS  Google Scholar 

  • Galeano CH, Fernández AC, Gómez M, Blair MW (2009a) Single strand conformation polymorphism based SNP and Indel markers for genetic mapping and synteny analysis of common bean (Phaseolus vulgaris L.). BMC Genomics 10:629

    Article  PubMed  Google Scholar 

  • Galeano CH, Gomez M, Rodriguez LM, Blair MW (2009b) CEL I nuclease for SNP discovery and marker development in common bean (Phaseolus vulgaris L.). Crop Sci 49:381–394

    Article  CAS  Google Scholar 

  • Gelin JR, Forster S, Grafton KF, McClean P, Rojas-Cifuentes GA (2007) Analysis of seed-zinc and other nutrients in a recombinant inbred population of navy bean (Phaseolus vulgaris L.). Crop Sci 47:1361–1366

    Article  CAS  Google Scholar 

  • Graham RD, Welch RM, Bouis HE (2001) Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: principals, perspectives and knowledge gaps. Adv Agron 70:77–144

    Article  Google Scholar 

  • Grusak MA (2002) Enhancing mineral content in plant food products. J Am Coll Nutr 21:178S–183S

    PubMed  Google Scholar 

  • Guzmán-Maldonado SH, Acosta-Gallegos JA, Paredes-López O (2000) Protein and mineral content of a novel collection of wild and weedy common bean (Phaseolus vulgaris L.). J Sci Food Agric 80:1874–1881

    Article  Google Scholar 

  • Guzman-Maldonado SH, Martínez O, Acosta-Gallegos J, Guevara-Lara FJ, Paredes-Lopez O (2003) Putative quantitative trait loci for physical and chemical components of common bean. Crop Sci 43:1029–1035

    Article  CAS  Google Scholar 

  • Hitz WD, Carlson TJ, Kerr PS, Sebastian SJ (2002) Biochemical and molecular characterization of a mutation that confers a decreased raffinosaccharide and phytic acid phenotype on soybean seeds. Plant Physiol 128:650–660

    Article  PubMed  CAS  Google Scholar 

  • Israel DW, Kwanyuen P, Burton JW (2006) Genetic variability for phytic acid phosphorus and inorganic phosphorus in seeds of soybeans in maturity groups V, VI, and VII. Crop Sci 46:67–71

    Article  CAS  Google Scholar 

  • Lander E, Green P, Abrahamson J, Barlow A, Daly M, Lincoln D, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Google Scholar 

  • Larson SR, Rutger JN, Young KA, Raboy V (2000) Isolation and genetic mapping of a non-lethal rice (Oryza sativa L.) low phytic acid 1 mutation. Crop Sci 40:1397–1405

    Article  CAS  Google Scholar 

  • Loewus FA, Murthy PPN (2000) myo-Inositol metabolism in plants. Plant Sci 150:1–19

    Article  CAS  Google Scholar 

  • Lolas G, Markakis P (1975) Phytic acid and others phosphorus compounds of beans (Phaseolus vulgaris L.). J Agric Food Chem 23:1094–1097

    Article  Google Scholar 

  • Lott JNA, Ockenden I, Raboy V, Batten GD (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci Res 10:11–33

    CAS  Google Scholar 

  • Murray J, Larsen J, Michaels TE, Schaafsma A, Vallejos CE, Pauls KP (2002) Identification of putative genes in bean (Phaseolus vulgaris) genomic (Bng) RFLP clones and their conversion to STSs. Genome 45:1013–1024

    Article  PubMed  CAS  Google Scholar 

  • Nelson JC (1997) QGENE: software for marker-based genomic analysis and breeding. Mol Breed 3:229–235

    Google Scholar 

  • Ochoa IE, Blair MW, Lynch JP (2006) QTL analysis of adventitious root formation in common bean (Phaseolus vulgaris L.) under contrasting phosphorus availability. Crop Sci 46:1609–1621

    Article  CAS  Google Scholar 

  • Oltmans SE, Fehr WR, Welke GA, Raboy V, Peterson KL (2005) Agronomic and seed traits of soybean lines with low-phytate phosphorus. Crop Sci 45:593–598

    Article  CAS  Google Scholar 

  • Panzeri D, Cassani E, Doria E, Tagliabue G, Forti L, Campion B, Bollini R, Brearley CA, Pilu R, Nielsen E, Sparvoli F (2011) A defective ABC transporter of the MRP family, responsible for the bean lpa1 mutation, affects the regulation of the phytic acid pathway, reduces seed myo-inositol and alters ABA sensitivity. New Phytol 191:70–83. doi:10.1111/j.1469-8137.2011.03666.x

    Article  PubMed  CAS  Google Scholar 

  • Pedrosa A, Vallejos CE, Bachmair A, Schweizer D (2003) Integration of common bean (Phaseolus vulgaris L.) linkage and chromosomal maps. Theor Appl Genet 106:205–212

    PubMed  CAS  Google Scholar 

  • Petry N, Egli I, Zeder C, Walczyk T, Hurrell R (2010) Polyphenols and phytic acid contribute to the low iron bioavailability from common beans in young women. J Nutr 22:1977–1982

    Google Scholar 

  • Pilu R, Panzeri D, Gavazzi G, Rasmussen SK, Consonni G, Nielsen E (2003) Phenotypic, genetic and molecular characterization of a maize low phytic acid mutant (lpa241). Theor Appl Genet 107:980–987

    Article  PubMed  CAS  Google Scholar 

  • Raboy V (2002) Progress in breeding low phytate crops. J Nutr 132:503–505

    Google Scholar 

  • Raboy V (2003) myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochemistry 64:1033–1043

    Article  PubMed  CAS  Google Scholar 

  • Raboy V (2007) The ABCs of low-phytate crops. Nat Biotechnol 25:874–875

    Article  PubMed  CAS  Google Scholar 

  • Raboy V, Bowen D (2006) Genetics of inositol polyphosphates. In: Lahiri Majumder A, Biswas BB (eds) Biology of inositols and phosphoinositides, pp 71–102

  • Raboy V, Dickinson DB (1984) Effect of phosphorus and zinc nutrition on soybean seed phytic acid and zinc. Plant Physiol 75:1094–1098

    Article  PubMed  CAS  Google Scholar 

  • Raboy V, Dickinson DB (1993) Phytic acid levels in seeds of Glycine max and G. soja as influenced by phosphorus status. Crop Sci 33:1300–1305

    Article  CAS  Google Scholar 

  • Raboy V, Dickinson DB, Below FE (1984) Variation in seed total phosphorus, phytic acid, zinc, calcium, magnesium and protein among lines of Glycine max and G. soja. Crop Sci 24:431–434

    Article  CAS  Google Scholar 

  • Raboy V, Young KA, Dorsch JA, Cook A (2001) Genetics and breeding of seed phosphorus and phytic acid. J Plant Physiol 158:489–497

    Article  CAS  Google Scholar 

  • Sandberg A-S, Brune M, Carlsson NG, Hallberg L, Skoglund E, Rossander-Hulthén L (1999) Inositol phosphates with different numbers of phosphate groups influence iron absorption in humans. Am J Clin Nutr 70:240–246

    PubMed  CAS  Google Scholar 

  • Stangoulis JC, Huynh BL, Welch RM, Choi E, Graham RD (2006) Quantitative trait loci for phytate in rice grain and their relationship with grain micronutrient content. Euphytica 154:289–294

    Article  Google Scholar 

  • Stevenson-Paulik J, Bastidas RJ, Chiou S-T, Frye RA, York RA (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci USA 102:12612–12617

    Article  PubMed  CAS  Google Scholar 

  • Tar’an B, Michaels T, Pauls P (2002) Genetic mapping of agronomic traits in common bean. Crop Sci 42:544–556

    Article  Google Scholar 

  • Voorips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  Google Scholar 

  • Walker DR, Scaboo AM, Pantalone VR, Wilcox JR, Boerma HR (2006) Genetic mapping of loci associated with seed phytic acid content in CX1834-1-2 soybean. Crop Sci 46:390–397

    Article  CAS  Google Scholar 

  • Wang TL, Domoney C, Hedley CL, Casey R, Grusak MA (2003) Can we improve the nutritional quality of legume seeds? Plant Phys 131:886–891

    Google Scholar 

  • Welch RM, House WA, Beebe S, Cheng Z (2000) Genetic selection for enhanced bioavailable levels of iron in bean (Phaseolus vulgaris L.). J Agric Food Chem 48:3576–3580

    Article  PubMed  CAS  Google Scholar 

  • Yu K, Park SJ, Poysa V, Gepts P (2000) Integration of simple sequence repeat (SSR) markers into a molecular linkage map of common bean (Phaseolus vulgaris L.). J Hered 91:429–434

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Genetics and Plant Breeding, Cornell University, 242 Emerson Hall, Ithaca, NY, 14853, USA

    Matthew W. Blair

  2. Department of Agronomy, Ohio State University, Wooster, OH, USA

    Andrea Lorena Herrera

  3. Department of Biology, University of Javeriana, Av. 7ta, Bogotá, Colombia

    Tito Alejandro Sandoval

  4. Department of Biochemistry and Molecular Biology, Colorado State University, 1970 Campus Delivery, Fort Collins, CO, USA

    Gina Viviana Caldas

  5. Instituto di Biologia e Biotecnolgia Agraria, CNR, Via Bassini 15, Milan, Italy

    Marizia Filleppi & Francesca Sparvoli

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  1. Matthew W. Blair
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  2. Andrea Lorena Herrera
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  3. Tito Alejandro Sandoval
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  4. Gina Viviana Caldas
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  5. Marizia Filleppi
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  6. Francesca Sparvoli
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Correspondence to Matthew W. Blair.

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Blair, M.W., Herrera, A.L., Sandoval, T.A. et al. Inheritance of seed phytate and phosphorus levels in common bean (Phaseolus vulgaris L.) and association with newly-mapped candidate genes. Mol Breeding 30, 1265–1277 (2012). https://doi.org/10.1007/s11032-012-9713-z

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