Abstract
Seed nutrients in legumes are important for human health, particularly in developing countries with heavy reliance on plant-based diets, and among vegetarians in developed nations. Here, we report on our efforts to uncover the genetic basis underlying the phenotypic variation for protein, zinc, calcium concentrations, and iron bioavailability present in 206 accessions of dry bean (Phaseolus vulgaris L.) from the Andean Diversity Panel (ADP). We used 8111 single nucleotide polymorphisms (SNPs) generated with genotyping-by-sequencing (GBS) to examine the allelic variants’ associations with seed protein, zinc, and calcium concentrations, and iron bioavailability in the 206 ADP accessions grown over 2 years in Michigan. These efforts identified phenotypic variation among the ADP genotypes for each of the traits, with the highest variation (5.4-fold) found for cooked seed iron bioavailability. In addition, significant SNP-trait associations were found and explained from 6.3 to 13.2% of the phenotypic variation. These results expand the current understanding of the genetic architecture underlying these complex nutritional quality traits and iron bioavailability in dry beans. Furthermore, they have utility for future nutritional quality breeding efforts to better biofortify dry bean through genomics-assisted breeding.
Similar content being viewed by others
Abbreviations
- ADP:
-
Andean diversity panel
- BLASTN:
-
Basic local alignment search tool for nucleotides
- FeBIO:
-
Iron bioavailability
- GBS:
-
Genotyping-by-sequencing
- GLM:
-
General linear model
- GWAS:
-
Genome-wide association study
- LD:
-
Linkage disequilibrium
- MLM:
-
Mixed linear model
- PCA:
-
Principal component analysis
- Pv:
-
Phaseolus vulgaris chromosome
- QTL:
-
Quantitative trait loci
- RILs:
-
Recombinant inbred lines
- SNP:
-
Single nucleotide polymorphism
References
Akibode CS, Maredia M (2011) Global and regional trends in production, trade and consumption of food legume crops. Report submitted to the Standing panel on impact assessment (SPIA) of the CGIAR Science Council, FAO, Rome
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
AOAC (1980) Official methods of analysis, 11th edn. Association of Official Analytical, Chemists, Washington, D.C
Asif M, Rooney LW, Ali R, Riaz MN (2013) Application and opportunities of pulses in the food system: a review. Crit Rev Food Sci Nutr 53:1168–1179. https://doi.org/10.1080/10408398.2011.574804
Astudillo-Reyes A, Fernandez AC, Cichy KA (2015) Transcriptome characterization of developing bean (Phaseolus vulgaris L.) pods from two genotypes with contrasting seed zinc concentrations. PLoS ONE 10:e0137157. https://doi.org/10.1371/journal.pone.0137157
Bass JK, Chan GM (2006) Calcium nutrition and metabolism during infancy. Nutr 22:1057–1066
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beebe SE (2012) Common bean breeding in the tropics. Plant Breed Rev 36:357–426. https://doi.org/10.1002/9781118358566.ch5
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J (2008) Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371:243–260. https://doi.org/10.1016/s0140-6736(07)61690-0
Blair MW, Izquierdo P (2012) Use of the advanced backcross-QTL method to transfer seed mineral accumulation nutrition traits from wild to Andean cultivated common beans. Theor Appl Genet 125:1015–1031. https://doi.org/10.1007/s00122-012-1891-x
Blair MW, Astudillo C, Grusak MA, Graham R, Beebe SE (2009a) Inheritance of seed iron and zinc concentrations in common bean (Phaseolus vulgaris L.) Mol Breed 23:197–207. https://doi.org/10.1007/s11032-008-9225-z
Blair MW, Sandoval TA, Caldas GV, Beebe SE, Paez MI (2009b) Quantitative trait locus analysis of seed phosphorus and seed phytate content in a recombinant inbred line population of common bean. Crop Sci 49:237–246. https://doi.org/10.2135/cropsci2008.05.0246
Blair MW, Medina JI, Astudillo C, Rengifo J, Beebe SE, Machado G, Graham R (2010a) QTL for seed iron and zinc concentration and content in a Mesoamerican common bean (Phaseolus vulgaris L.) population. Theor Appl Genet 121:1059–1070. https://doi.org/10.1007/s00122-010-1371-0
Blair MW, Gonzalez LF, Kimani PM, Butare L (2010b) Genetic diversity, inter-gene pool introgression and nutritional quality of common beans (Phaseolus vulgaris L.) from Central Africa. Theor Appl Genet 121:237–248. https://doi.org/10.1007/s00122-010-1305-x
Blair MW, Astudillo C, Rengifo J, Beebe SE, Graham R (2011) QTL analyses for seed iron and zinc concentrations in an intra-gene pool population of Andean common beans (Phaseolus vulgaris L.) Theor Appl Genet 122:511–521. https://doi.org/10.1007/s00122-010-1465-8
Blair MW, Herrera AL, Sandoval TA, Caldas GV, Filleppi M, Sparvoli F (2012) Inheritance of seed phytate and phosphorus levels in common bean (Phaseolus vulgaris L.) and association with newly-mapped candidate genes. Mol Breed 30:1265–1277. https://doi.org/10.1007/s11032-012-9713-z
Blair MW, Wu X, Bhandari D, Astudillo C (2016) Genetic dissection of ICP-detected nutrient accumulation in the whole seed of common bean (Phaseolus vulgaris L.) Front Plant Sci 7:219–217. https://doi.org/10.3389/fpls.2016.00219
Boccio JR, Iyengar V (2003) Iron deficiency: causes, consequences, and strategies to overcome this nutritional problem. Biol Trace Elem Res 94:1–32
Bouain N, Shahzad Z, Rouached A, Khan GA, Berthomieu P, Abdelly C, Poirier Y, Rouached H (2014) Phosphate and zinc transport and signalling in plants : towards a better understanding of their homeostasis interaction. J Exp Bot 65:5725–5741. https://doi.org/10.1093/jxb/eru314
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. https://doi.org/10.1093/bioinformatics/btm308
Bremner JM (1965) Total nitrogen. In: Black CA et al (eds) Methods of soil analysis. Part 2. Agron Monogr 9. ASA, Madison, pp 1149–1178
Brinch-Pedersen H, Borg S, Tauris B, Holm PB (2007) Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J Cereal Sci 46:308–326. https://doi.org/10.1016/j.jcs.2007.02.004
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702. https://doi.org/10.1111/j.1469-8137.2007.01996.x
Caballero B (2002) Global patterns of child health: the role of nutrition. Ann Nutr Metab 46:3–7
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. https://doi.org/10.1007/s00122-009-0975-8
Campion B, Glahn RP, Tava A, Perrone D, Doria E, Sparvoli F, Cecotti R, Dani V, Nielsen E (2013) Genetic reduction of antinutrients in common bean (Phaseolus vulgaris L.) seed, increases nutrients and invitro iron bioavailability without depressing main agronomic traits. Field Crops Res 141:27–37. https://doi.org/10.1016/j.fcr.2012.10.015
Casanas F, Perez-Vega E, Almirall A, Plans M, Sabate J, Ferreira JJ (2013) Mapping of QTL associated with seed chemical content in a RIL population of common bean (Phaseolus vulgaris L.) Euphytica 192:279–288. https://doi.org/10.1007/s10681-013-0880-8
Cichy KA, Caldas GV, Snapp SS, Blair MW (2009a) QTL analysis of seed iron, zinc, and phosphorus levels in an Andean bean population. Crop Sci 49:1742–1750. https://doi.org/10.2135/cropsci2008.10.0605
Cichy KA, Blair MW, Mendoza CHG, Snapp SS, Kelly JD (2009b) QTL analysis of root architecture traits and low phosphorus tolerance in an Andean bean population. Crop Sci 49:59–68. https://doi.org/10.2135/cropsci2008.03.0142
Cichy KA, Porch TG, Beaver JS, Cregan P, Fourie D, Glahn RP, Grusak MA, Kamfwa K, Katuuramu DN, McClean P, Mndolwa E, Nchimbi-Msolla S, Pastor-Corrales MA, Miklas PN (2015a) A Phaseolus vulgaris diversity panel for Andean bean improvement. Crop Sci 55:2149–2160. https://doi.org/10.2135/cropsci2014.09.0653
Cichy KA, Wiesinger JA, Mendoza FA (2015b) Genetic diversity and genome-wide association analysis of cooking time in dry bean (Phaseolus vulgaris L.) Theor Appl Genet 128:1555–1567. https://doi.org/10.1007/s00122-015-2531-z
Darnton-Hill I, Webb P, Harvey PW, Hunt JM, Dalmiya N, Chopra M, Ball MJ, Bloem MW, de Benoist B (2005) Micronutrient deficiencies and gender: social and economic costs. Am J Clin Nutr 81:S1198–S1205
Delaney DE, Bliss FA (1991) Selection for increased percentage phaseolin in common bean: 1. Comparison of selection for seed protein alleles and S1 family recurrent selection. Theor Appl Genet 81:301–305. https://doi.org/10.1007/bf00228667
Duranti M, Gius C (1997) Legume seeds: protein content and nutritional value. Field Crops Res 53:31–45. https://doi.org/10.1016/s0378-4290(97)00021-x
Ekmekcioglu C, Elmadfa I, Meyer AL, Moeslinger T (2016) The role of dietary potassium in hypertension and diabetes. J Physiol Biochem 72:93–106. https://doi.org/10.1007/s13105-015-0449-1
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high density species. PLoS One 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Endelman JB, Jannink JL (2012) Shrinkage estimation of the realized relationship matrix. G3:Genes Genomes Genet 2:1405–1413. https://doi.org/10.1534/g3.112.004259
Farnham MW, Keinath AP, Grusak MA (2011) Mineral concentration of Broccoli florets in relation to year of cultivar release. Crop Sci 51:2721–2727. https://doi.org/10.2135/cropsci2010.09.0556
Fileppi M, Galasso I, Tagliabue G, Daminati MG, Campion B, Doria E, Sparvoli F (2010) Characterization of structural genes involved in phytic acid biosynthesis in common bean (Phaseolus vulgaris L.) Mol Breed 25:453–470. https://doi.org/10.1007/s11032-009-9344-1
Gao Y, Shang C, Maroof MAS, Biyashev RM, Grabau EA, Kwanyuen P, Burton JW, Buss GR (2007) A modified colorimetric method for phytic acid analysis in soybean. Crop Sci 47:1797–1803. https://doi.org/10.2135/cropsci2007.03.0122
Ghosh S, Suri D, Uauy R (2012) Assessment of protein adequacy in developing countries: quality matters. Brit J Nutr 108(S2):S77–S87
Gibson RS (2006) Zinc: the missing link in combating micronutrient malnutrition in developing countries. Proc Nutr Soc 65:51–60. https://doi.org/10.1079/pns2005474
Glahn RP, Lee OA, Yeung A, Goldman MI, Miller DD (1998) Caco-2 cell ferritin formation predicts non-radiolabeled food iron availability in an in vitro digestion/ Caco-2 cell culture model. J Nutr 128:1555–1561
Glaubitz JC, Casstevens TM, Liu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9:e90346. https://doi.org/10.1371/journal.pone.0090346
Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944
Guzman-Maldonado SH, Martinez O, Acosta-Gallegos JA, Guevara-Lara F, Paredes-Lopez O (2003) Putative quantitative trait loci for physical and chemical components of common bean. Crop Sci 43:1029–1035. https://doi.org/10.2135/cropsci2003.1029
Hart JP, Griffiths PD (2015) Genotyping-by-sequencing enabled mapping and marker development for the By-2 potyvirus resistance allele in common bean. Plant Gen 8. doi:https://doi.org/10.3835/plantgenome2014.09.0058
Hart JJ, Elad T, Kochian LV, Glahn RP (2015) Identification of black bean (Phaseolus vulgaris L.) polyphenols that inhibit and promote iron uptake by Caco-2 cells. J Agric Food Chem 63:5950–5956. https://doi.org/10.1021/acs.jafc.5b00531
Hart JJ, Elad T, Glahn RP (2017) Characterization of polyphenol effects on inhibition and promotion of iron uptake by Caco-2 cells. J Agric Food Chem 65:3285–3294. https://doi.org/10.1021/acs.jafc.6b05755
Hirschi KD (2009) Nutrient biofortification of food crops. Annu Rev Nutr 29:401–421
Houston MC (2011) The importance of potassium in managing hypertension. Curr Hypertens Rep 13:309–317. https://doi.org/10.1007/s11906-011-0197-8
Hu Y, Cheng Z, Heller LI, Krasnoff SB, Glahn RP, Welch RM (2006) Kaempferol in red and pinto bean (Phaseolus vulgaris L.) coats inhibits iron bioavailability using an in vitro digestion/ human Caco-2 cell model. 54:9254–9261
Ibarra-Perez FJ, Ehdaie B, Waines JG (1997) Estimation of outcrossing rate in common bean. Crop Sci 37:60–65. https://doi.org/10.2135/cropsci1997.0011183X003700010009x
Ingvarsson PK, Street NR (2011) Association genetics of complex traits in plants. New Phytol 189:909–922. https://doi.org/10.1111/j.1469-8137.2010.03593.x
Islam FMA, Basford KE, Jara C, Redden RJ, Beebe SE (2002a) Seed compositional and disease resistance differences among gene pools in cultivated common bean. Genet Resour Crop Evol 49:285–293. https://doi.org/10.1023/a:1015510428026
Islam FMA, Basford KE, Redden RJ, Gonzalez AV, Kroonenberg PM, Beebe SE (2002b) Genetic variability in cultivated common bean beyond the two major gene pools. Genet Resour Crop Evol 49:271–283. https://doi.org/10.1023/a:1015567513005
Kamfwa K, Cichy KA, Kelly JD (2015) Genome-wide assocaition analysis of symbiotic nitorgen fixation in common bean. Theor Appl Genet 128:1999–2017. https://doi.org/10.1007/s00122-015-2562-5
Katungi E, Farrow A, Chianu J, Sperling L, Beebe S (2009) Common bean in eastern and southern Africa: a situation and outlook analysis. International Centre for Tropical Agriculture, CIAT 61
Kwak M, Gepts P (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor Appl Genet 118:979–992
Latta M, Eskin M (1980) A simple and rapid colorimetric method for phytate determination. J Agric Food Chem 28:1313–1315. https://doi.org/10.1021/jf60232a049
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
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 https://doi.org/10.1017/S0960258500000039
Ma Y, Bliss FA (1978) Seed proteins of common bean. Crop Sci 18:431–437
Manach C, Scalbert A, Morand C, Remsey C, Jimenez L (2004) Polyphenols: food sources and bioavailability. Amer J Clin Nutr 79:727–747
Matsumoto T, Wu JZ, Kanamori H, Katayose Y, Fujisawa M, Namiki N et al (2005) The map-based sequence of the rice genome. Nature 436:793–800. https://doi.org/10.1038/nature03895
Messina V (2014) Nutritional and health benefits of dried beans. Am J Clin Nutr 100:437S–442S. https://doi.org/10.3945/ajcn.113.071472
Miller R, Spiro A, Stanner S (2016) Micronutrient status and intake in the UK - where might we be in 10 years’ time? Nutr Bull 41:14–41. https://doi.org/10.1111/nbu.12187
Millward DJ, Jackson AA (2004) Protein/energy ratios of current diets in developed and developing countries compared with a safe protein/energy ratio: implications for recommended protein and amino acid intakes. Public Health Nutr 7:387–405. https://doi.org/10.1079/phn2003545
Mitchell DC, Lawrence FR, Hartman TJ, Curran JM (2009) Consumption of drybeans, peas, and lentils could improve diet quality in the U.S population. J Am Diet Assoc 109:909–913. https://doi.org/10.1016/j.jada.2009.02.029
Moraghan JT, Grafton K (2001) Genetic diversity and mineral composition of common bean seed. J Sci Food Agric 81:404–408. https://doi.org/10.1002/1097-0010(200103)81:4<404::AID-JSFA822>3.0.CO;2-H
Mudryj AN, Yu N, Aukema HM (2014) Nutritional and health benefits of pulses. Appl Physiol Nutr Metab 39:1197–1204. https://doi.org/10.1139/apnm-2013-0557
O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX, Hernandez G, Vance CP (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genomics 15:866–881
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. https://doi.org/10.1111/j.1469-8137.2011.03666.x
Perochon A, Aldon D, Galaud JP, Ranty B (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93:2048–2053. https://doi.org/10.1016/j.biochi.2011.07.012
Petry N, Egli I, Gahutu JB, Tugirimana PL, Boy E, Hurrell R (2012) Stable iron isotope studies in Rwandese women indicate that the common bean has limited potential as a vehicle for iron biofortification. J Nutr 142:492–497
Pinheiro C, Baeta JP, Pereira AM, Domingues H, Ricardo CP (2010) Diversity of seed mineral composition of Phaseolus vulgaris L. germplasm. J Food Compos Anal 23:319–325. https://doi.org/10.1016/j.jfca.2010.01.005
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. https://doi.org/10.1038/ng1847
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 Glycine soja. Crop Sci 24:431–434. https://doi.org/10.2135/cropsci1984.0011183X002400030001x
Rhee SY, Beavis W, Berardini TZ, Chen GH, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, Mueller LA, Mundodi S, Reiser L, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31:224–228. https://doi.org/10.1093/nar/gkg076
Rizzoli R, Boonen S, Brandi ML, Burlet N, Delmas P, Reginster JY (2008) The role of calcium and vitamin D in the management of osteoporosis. Bone 42:246–249. https://doi.org/10.1016/j.bone.2007.10.005
Rodgers A, Ezzati M, Hoorn SV, Lopez AD, Lin RB, Murray CJL et al (2004) Distribution of major health risks: findings from the global burden of disease study. PLoS Med 1:44–55. https://doi.org/10.1371/journal.pmed.0010027
SAS Institute (2011) SAS Version 9.4 SAS Institute Inc Cary, NC.
Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670
Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713. https://doi.org/10.1038/ng.3008
Schröder S, Mamidi S, Lee R et al (2016) Optimization of genotyping by sequencing (GBS) data in common bean (Phaseolus vulgaris L.) Mol Breed 36:1–9
Song Q, Jia G, Hyten DL, Jenkins J, Hwang EY, Schroeder SG, Osorno JM, Schmutz J, Jackson SA, McClean PE, Cregan PB (2015) SNP Assay Development for linkage map construction, anchoring whole-genome sequence, and other genetic and genomic applications in common bean. G3: Genes Genomes Genet 5:2285–2290. https://doi.org/10.1534/g3.115.020594
Stein AJ (2010) Global impacts of human mineral malnutrition. Plant Soil 335:133–154. https://doi.org/10.1007/s11104-009-0228-2
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. PNAS 100:9440–9445
Swarts K, Li H, Romero JA, Navarro D, Romay MC, Hearne S et al (2014) Novel methods to optimize genotypic imputation for low-coverage, next-generation sequence data in crop plants. Plant G E N 7:3–14. https://doi.org/10.3835/plantgenome2014.05.0023
Tako E, Glahn RP (2011) White beans provide more bioavailable iron than red beans: studies in poultry (Gallus gallus) and an in vitro digestion/ Caco-2 model. Int J Vitam Nutr Res 81:1–14. https://doi.org/10.1024/0300-9831/a000028
Tako E, Blair MW, Glahn RP (2011) Biofortified red mottled beans (Phaseolus vulgaris L.) in maize and bean diet provide more bioavailable iron than standard red mottled beans: studies in poultry (Gallus gallus) and an in vitro digestion/ Caco-2 model. Nutr J 10:113–123. https://doi.org/10.1186/1475-2891-10-113
Tako E, Beebe SE, Reed S, Hart JJ, Glahn RP (2014) Polyphenolic compounds appear to limit the nutritional benefit of biofortified higher iron black bean (Phaseolus vulgaris L.) J Nutr 13:28–37. https://doi.org/10.1186/1475-2891-13-28
Turner SD (2014) Qqman: an R package for visualizing GWAS results using Q-Q and Manhattan plots. https://www.biorxiv.org
U.S. Department of Agriculture and U.S. Department of Health and Human Services (2011) Report of the dietary guidelines for Americans, 7th edn. U.S. Government Printing Office, Washington, D.C
Wang N, Daun JK (2005) Determination of cooking times of pulses using an automated Mattson cooker apparatus. J Sci Food Agric 85:1631–1635
Weaver CM (2013) Potassium and health. Adv Nutr 4:368S–377S. https://doi.org/10.3945/an.112.003533
White PJ (2013) Improving potassium acquisition and utilization by crop plants. J Plant Nutr Soil Sci 176:305–316. https://doi.org/10.1002/jpln.201200121
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511. https://doi.org/10.1093/aob/mcg/164
Wiesinger JA, Cichy KA, Glahn RP, Grusak MA, Brick MA, Thompson HJ, Tako E (2016) Demonstrating a nutritional advantage to the fast-cooking dry bean (Phaseolus vulgaris L.) J Agric Food Chem 64:8592–8603
Williams LE, Mills RF (2005) P(1B)-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502. https://doi.org/10.1016/j.tplants.2005.08.008
Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208. https://doi.org/10.1038/ng1702
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. https://doi.org/10.1038/ng.546
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Gen 1:5–20. https://doi.org/10.3835/plantgenome2008.02.0089
Zimmermann MB, Hurrell RF (2007) Nutritional iron deficiency. Lancet 370:511–520
Acknowledgements
We thank the Feed the Future Norman Borlaug Commemorative Research Initiative (NBCRI) Grain Legumes Project, a research partnership between US Agency for International Development (USAID) and the USDA-ARS, and the Feed the Future Innovation Lab for Collaborative Research on Grain Legumes by USAID as part of Feed the Future US Government’s global hunger and food security initiative, under the terms of Cooperative Agreement No. EDH-A-00-07-00005-00, for financial support. The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.
Author information
Authors and Affiliations
Contributions
DNK designed the experiments, collected and analyzed data, and wrote the manuscript. JPH conducted genotyping and SNP calling and wrote manuscript. TGP conducted genotyping and reviewed the manuscript. MAG conducted mineral analysis and reviewed the manuscript. RPG conducted iron bioavailability analysis and reviewed the manuscript. KAC designed the experiments, collected data, and wrote and edited the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Supplemental Table S1
List of all Andean Diversity Panel dry bean genotypes and genotype by sequencing key (XLS 329 kb)
Supplemental Figure S1
Histogram showing the distribution of seed protein, zinc, iron, and iron bioavailability in the cooked dry bean seed samples of 206 ADP genotypes that were grown in Michigan, USA for two field seasons (PNG 233 kb)
Supplemental Figure S2
Histogram showing the distribution of seed potassium, calcium, phosphorus, and phytic acid concentration in the cooked dry bean seed samples of 206 ADP genotypes that were grown in Michigan, USA for two field seasons (PNG 224 kb)
Supplemental Figure S3
GLM-based Manhattan plots depicting genome-wide marker-trait association in cooked dry bean seeds protein concentration (A), zinc concentration (C), calcium concentration (E), and iron bioavailability (G) The cutoff (red horizontal line) is based on the qFDR ≤ 0.1 used to declare genome-wide significance. The Quantile-Quantile plots testing for model goodness of fit and SNP marker inflation of the GLM model of cooked dry bean seed samples for protein concentration (B), zinc concentration (D), calcium concentration (F), and iron bioavailability (H) are also provided. (PNG 1437 kb)
Rights and permissions
About this article
Cite this article
Katuuramu, D.N., Hart, J.P., Porch, T.G. et al. Genome-wide association analysis of nutritional composition-related traits and iron bioavailability in cooked dry beans (Phaseolus vulgaris L.). Mol Breeding 38, 44 (2018). https://doi.org/10.1007/s11032-018-0798-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-018-0798-x