Article pubs.acs.org/JAFC
Demonstrating a Nutritional Advantage to the Fast-Cooking Dry Bean (Phaseolus vulgaris L.) Jason A. Wiesinger,† Karen A. Cichy,*,†,‡ Raymond P. Glahn,§ Michael A. Grusak,⊗ Mark A. Brick,⊥ Henry J. Thompson,# and Elad Tako§ †
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, Michigan 48824, United States USDA-ARS, Sugarbeet and Bean Research Unit, Michigan State University, East Lansing, Michigan 48824, United States § USDA-ARS, Robert W. Holley Center for Agriculture and Health, Cornell University, Ithaca, New York 14853, United States ⊗ USDA-ARS, Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030, United States ⊥ Department of Soil and Crop Sciences, Colorado State University, Fort Collins, Colorado 80523, United States # Department of Horticulture and Landscape Architecture, Colorado State University, Fort Collins, Colorado 80523, United States ‡
S Supporting Information *
ABSTRACT: Dry beans (Phaseolus vulgaris L.) are a nutrient-dense food rich in protein and micronutrients. Despite their nutritional benefits, long cooking times limit the consumption of dry beans worldwide, especially in nations where fuelwood for cooking is often expensive or scarce. This study evaluated the nutritive value of 12 dry edible bean lines that vary for cooking time (20−89 min) from four market classes (yellow, cranberry, light red kidney, and red mottled) of economic importance in bean-consuming regions of Africa and the Americas. When compared to their slower cooking counterparts within each market class, fast-cooking dry beans retain more protein and minerals while maintaining similar starch and fiber densities when fully cooked. For example, some of the highest protein and mineral retention values were measured in the fast-cooking yellow bean cultivar Cebo Cela, which offered 20% more protein, 10% more iron, and 10% more zinc with each serving when compared with Canario, a slow-cooking yellow bean that requires twice the cooking time to become palatable. A Caco-2 cell culture model also revealed the bioavailability of iron is significantly higher in faster cooking entries (r = −0.537, P = 0.009) as compared to slower cooking entries in the same market class. These findings suggest that fast-cooking bean varieties have improved nutritive value through greater nutrient retention and improved iron bioavailability. KEYWORDS: dry beans, Phaseolus vulgaris L., cooking time, protein, iron, zinc, phytate, Caco2 cell culture, iron bioavailability
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INTRODUCTION Dry beans (Phaseolus vulgaris L.) are a major pulse crop used for direct human consumption. Their capacity for symbiotic nitrogen fixation contributes to their nutrient density but also makes them ideal for low-input agricultural systems practiced by smallholder farmers in Africa, Latin America, and the Caribbean.1,2 Dry beans are protein rich: in one half-cup serving, cooked dry beans provide 3 times as much protein as a comparable serving of maize (Zea mays L.) and 25% of the daily requirement for lysine as estimated for a 60 kg person.3−5 In Latin America, 10−15% of protein intake over the course of a day comes from the consumption of dry beans. In parts of East Africa, they contribute as much as 55% of the daily intake of protein.6 Dry beans are also a rich source of minerals including iron and zinc.7 In an effort to alleviate malnutrition in regions where edible beans are consumed routinely, they are considered an excellent crop for trace mineral biofortification.2,8,9 An estimated 17.3% of the world population has inadequate zinc intake, with the greatest prevalence in regions of Sub-Saharan Africa.10 Approximately 24% of the world’s population is believed to be suffering from anemia, with the highest incidences in Africa and Asia.11 Improved nutritive value has © 2016 American Chemical Society
increasingly become a consideration of breeding programs in numerous crops.12,13 In dry bean, breeding has increased seed iron levels to 80% higher than standard varieties.14 New cultivars of high mineral accumulating beans have already been released in parts of Africa.8,15 Despite their abundant density of minerals, the bioavailability of iron and zinc in dry beans is often limited by the large amounts of dietary inhibitors, such as phytates and tannins.16−18 When compared to the other staple food crops of rice and maize, dry beans require relatively longer cooking times to inactivate the amylase/trypsin inhibitors, solubilize fiber, denature storage proteins, and gelatinize the granules of starch prior to consumption.19 As the seed ages, or is exposed to higher ambient temperatures and humidity, the cooking time increases.20,21 Longer cooking times restrict bean consumption, especially in regions where the use of energy plays a pivotal role in the selection of foods needed for meal preparation. A large proportion of the world’s rural population (∼2 billion) uses Received: Revised: Accepted: Published: 8592
July 12, 2016 October 3, 2016 October 18, 2016 October 18, 2016 DOI: 10.1021/acs.jafc.6b03100 J. Agric. Food Chem. 2016, 64, 8592−8603
Article
Journal of Agricultural and Food Chemistry
Table 1. Description, Collection Sites, and Agricultural Attributes of the 12 Accession Entries That Characterize the Health & Nutrition Panela market class
entry
collection site
attributes
yellow
Cebo Cela Uyole 98 Canario
Angola Tanzania Angola
collected from marketplace in 2010 excellent palatability, strong agronomical traits, anthracnose resistance collected from marketplace in 2010
cranberry
G23086 OPS-RS4 Katarina Kibala
Malawi South Africa Angola
landrace collected in 1983, part of CIAT core collection yield stability, BCMV resistance, rust tolerance (Uromyces appendiculatus) collected from marketplace in 2010
red mottled
JB178 Vazon-7 PR0737-1
Puerto Rico Puerto Rico Puerto Rico
superior agricultural traits and disease resistance middle American landrace important in Caribbean agriculture strong agronomical traits with virus resistance
light red kidney
AC ELK Clouseau Pink Panther
Canada USA USA
commercial, high-yielding variety with superior canning qualities commercial, high-yielding variety with superior canning qualities commercial, high-yielding variety with superior canning qualities
a
The Health & Nutrition Panel consists of medium-size seeds ranging from 35 to 45 (g/100 seed) and large light red kidneys (60−70 g/100 seed). BCMV, bean common mosaic virus; CIAT, International Center of Tropical Agriculture. basis of a germplasm screening of over 200 P. vulgaris accessions from diverse geographic origins including Asia, the Americas, Africa, and Europe.29,30 A summary of the entries, seed collection sites, and important agricultural attributes of the HNP are presented in Table 1. The HNP includes three bean lines with a wide range of cooking times from four different market classes (yellow, cranberry, red mottled, light red kidney) of agricultural importance to eastern Africa, southern Africa, the Caribbean, and North America. The yellow and cranberry lines were collected from Africa. Cebo Cela, Canario, and Katarina Kibala were collected in the public markets of Angola, which attests to their consumer acceptability. Cultivar Uyole 98 was released in 1999 by the Tanzanian National breeding program to meet the quality standards of the East African marketplace.31 G23086 is a landrace collected from Malawi, and cv. OPS-RS4 is a cultivar released by the South Africa National Program in 2001 (D. Fourie, Agriculture Research Council, South Africa; personal communication). The three red mottled accessions are from the Caribbean. Red mottled beans are preferred seed types in the marketplaces of both the Caribbean and many parts of Africa. Cultivar JB178 was released in the Dominican Republic in 1998.32 Vazon-7 is an important Middle American landrace grown in the Caribbean.33 PR0737-1 is a virus-resistant line released jointly by the University of Puerto Rico, USDA-ARS, and Haiti National Program in 2013.34 The three light red kidney beans are high-yielding, commercially released varieties from North America that meet industry-defined standards for canning quality. Cultivar AC ELK was released by Agriculture and Agri-Food Canada in 1998.35 Clouseau was released as a patented cultivar in 2009, developed by Seminis Vegetable Seeds, Inc.36 Cultivar Pink Panther is a light red kidney released by Seminis Asgrow Research in 2003.37 Field Design and Storage Conditions. All accessions were planted in a randomized-complete-block design with two field replicates at the Michigan State University Montcalm Research Farm near Entrican, MI, USA, in 2012 and 2013.29 Field experimental units consisted of two rows 4.75 m long with 0.5 m spacing between rows. The soil type is Eutric Glossoboralfs (coarse-loamy, mixed) and Alfic Fragiorthods (coarse-loamy, mixed, frigid). Rainfall was supplemented with overhead irrigation as needed. No fertilizer was applied to the plots, and recommended practices were followed for weed and insect control. Seeds were harvested upon maturity by hand pulling the entire experimental unit and threshing with a Hege 140 plot harvester (Wintersteiger, UT, USA). Three weeks after harvest (designated “postharvest” in the results), 200 bean seeds from each field replicate of each entry in the HNP were hand selected to eliminate any external material and immature, wrinkled, discolored, or damaged seeds. To investigate seed changes after storage treatment, a subset of seed for each entry/replicate from field season 2012 was placed into dark
traditional biomass (fuelwood, charcoal, crop residues) for cooking and heating.22,23 Over 90% of East Africa and up to 60% of the rural population of Central and Latin America use solid fuels as the primary source of household energy.22,24,25 Furthermore, the process of purchasing or gathering solid fuels places a substantial burden on families as a time-consuming, labor-intensive task.26 The work of Brouwer et al. reports how the nutritional quality of meals is negatively affected when cooking energy becomes limited in rural households of Malawi.27,28 A fast-cooking dry bean has the potential to positively affect consumers by reducing fuelwood use and meal preparation time. The potential nutritional implications of fast-cooking bean varieties are not known. Fast-cooking beans may have intrinsic compositional differences that directly relate to their nutrient density. In addition, the varied time in the cooking process may influence nutrient retention and bioavailability. Cooking time is also a major aspect that industry must consider in processing bean products, as reducing cooking time could save energy resources needed in the canning process. The purpose of this study was to evaluate the associations between cooking time and composition of key dietary nutrients among a panel of 12 dry bean lines/cultivars. This panel was designed to include a wide range of cooking times from the major bean classes consumed in Africa, the Caribbean, and North America. The nutrient composition of the panel was evaluated soon after harvest, with cooking times in distilled water ranging from 20 to 68 min. The panel was also evaluated after a year of storage, when cooking times ranged from 26 to 89 min. Dietary inhibitors, such as phytate−protein−mineral interactions, were also considered in the examination of the nutritional value and health impacts between the fast and slower cooking genotypes of the panel. Using a Caco-2 cell culture model, the in vitro bioavailability of iron was also measured in the 12 genotypes postharvest and following storage.
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MATERIALS AND METHODS
Experiment Model: The Health & Nutrition Panel. The Health & Nutrition Panel (HNP) is composed of 12 edible dry bean lines/ cultivars that were carefully selected for nutritional evaluation on the 8593
DOI: 10.1021/acs.jafc.6b03100 J. Agric. Food Chem. 2016, 64, 8592−8603
Article
Journal of Agricultural and Food Chemistry storage under ambient conditions (20−25 °C, 50−60% relative humidity) at standard atmospheric pressure for 1 year. This sample set is designated “stored for 1 year” in the results. Cooking Time Determination. To equilibrate moisture content before soaking/cooking, all bean seeds collected after harvest and following storage treatment were stored within a controlled atmosphere cabinet (Storage Control Systems, Inc., Sparta, MI, USA) at room temperature over a saturated sodium nitrite salt solution (63% relative humidity) until seeds reached a moisture content of 10%.38 Prior to cooking, moisture-equilibrated bean seeds were soaked in distilled water (1:6 w/w) for 12 h at room temperature. Cooking time was determined using a Mattson pin drop cooking device.39,40 The cooker utilizes a rack of 25 stainless steel 70 g piercing rods placed in contact with the middle surface of a presoaked bean, which is fitted into a 4 L stainless steel beaker containing 1.8 L of boiling distilled water heated over a Waring SB30 portable burner. Cooking time was standardized as the number of minutes required for 80% of the 2 mm diameter piercing tip rods to pass completely through each seed under a low-steady boil (100 °C). Once removed from boiling water, samples were allowed to cool for 10 min at room temperature. The total number of 25 cooked seeds to fill a quarter cup was recorded and then doubled for serving-size determinations. Cooked samples, as well as raw seeds from each field replicate, were frozen and stored at −80 °C before freeze-drying (VirTis Research Equipment, Gardiner, NY, USA). For chemical analysis, 100 lyophilized raw and cooked seeds from each field replicate were preweighed, milled into fine powder (0.5 mm sieve), and then stored at 18 °C in sealed, opaque polypropylene plastic containers. Proximate Composition Analysis. Whole seed total nitrogen concentration was determined in 500 mg of lyophilized powder from each raw and cooked sample by the Dumas combustion method at A&L Great Lakes Laboratories (Fort Wayne, IN, USA) in accordance with AOAC method 968.06.41 The percentage of crude protein was estimated by multiplying the dry weight total nitrogen concentration by a factor of 6.25. A starch assay kit (K-STA; Megazyme International, Ireland) was used to measure total starch concentrations in 100 mg of lyophilized powder from raw and cooked samples with predissolution in cold 2 M KOH in accordance with AOAC method 996.11.41 Liberated glucose was quantified colorimetrically with glucose oxidase−peroxidase (GOPOD) reagent. Total starch was calculated with Mega-Calc against the absorbance of reagent blank and D-glucose standards read at a wavelength of 510 nm. Integrated total dietary fiber in 1 g of lyophilized powder from raw and cooked samples was measured using an adaptation of the AOAC 2011.25 Codex method with a commercial assay kit (K-INTDF; Megazyme International, Ireland) as described in detail in Kleintop et al.42 The assay includes enzymatic digestion with α-amylase/amyloglucosidase, two gravimetric filtrations, and high-performance liquid chromatography (HPLC) to quantify oligosaccharide concentrations.43,44 Moisture and ash were measured gravimetrically in 1 g of lyophilized powder from raw and cooked samples according to AOAC methods 925.09 and 923.03.41 Mineral Analysis. For mineral analysis, 500 mg of lyophilized powder from each raw and cooked sample was predigested overnight in borosilicate glass tubes with 3 mL of concentrated ultrapure nitric acid for 16 h at room temperature. Samples were then placed in a digestion block (Martin Machine, Ivesdale, IL, USA) and incubated for 4 h at 125 °C with refluxing. Subsequently, samples were cooled for 5 min before the addition of 2 mL of hydrogen peroxide and incubated at 125 °C for an additional hour. This step was repeated a second time before the digestion block temperature was raised to 200 °C; this temperature was maintained until each sample was completely dry. Digested samples were then resuspended in 2% ultrapure nitric acid and incubated overnight prior to analysis using inductively coupled plasma-optical emission spectroscopy (ICP-OES) (CIROS ICP model FCE12, Spectro, Kleve, Germany) with daily calibration of certified standards. To ensure batch-to-batch accuracy, all samples were digested and measured alongside tomato leaf standards purchased from the National Institute of Standards and Technology (SRM 1573A; Gaithersburg, MD, USA).
Phytate Determination. Phytic acid phosphorus (PA-P) was measured in 50 mg of lyophilized powder from raw and cooked samples using a modified colorimetric assay (Wade’s reagent).45 To calculate the phytate, PA-P (g/g) was multiplied by 3.55, which is a factor derived from the molecular weights of phosphorus (P, 31g/ mol), phytic acid (660 g/mol), and the molar ratio of P/phytic acid (6 mol/mol).46 phytate (g/g) =
PA‐P (g/g) × 660 g/mol 6 × 31 g/mol
The molar ratios between phytate (660g/mol), iron (56 g/mol), and zinc (65 g/mol) were calculated by dividing the moles of phytate by the moles of trace mineral. Nutritional Evaluation of the HNP. Three parameters were taken in consideration in the evaluation of the nutritive value of the HNP. (1) First, the concentration of a nutrient was determined in lyophilized powder representing a homogeneous mixture of either 100 raw or 100 cooked whole seeds and expressed as grams of nutrient per gram of 100 milled dried seed. (2) The nutrient content was calculated as grams of nutrient in 100 dried raw and cooked whole seeds, which accounts for bean entry differences for seed weight and sizes within the HNP. (3) Nutrient retention percentages were evaluated by comparing the total nutrient content between 100 raw and 100 cooked seeds. The content and nutrient retention, as well as serving size values, were calculated according to the following formulas: nutrient content = [nutrient concentration in lyophilized powder (g/g)] × [av wt of lyophilized powder that represents 100 raw or cooked whole seeds (g/100 seeds)]
% retention =
cooked nutrient content (g/100 seeds) × [100%] raw nutrient content (g/100 seeds)
serving size = [nutrient content (g/100 seeds)] × [no. of seeds per serving (half cup)] [100 seeds]
Iron Bioavailability: Caco-2 Cell Culture Assay. A 500 mg sample of lyophilized powder from cooked seed of each field replicate was subjected to an in vitro digestion/Caco-2 cell culture model for the measurement of iron bioavailability according to the detailed procedures previously described in Glahn et al.47 For comparisons between the different colored market classes, the increase in ferritin production is expressed relative to a cooked−lyophilized−finely milled Merlin white navy bean control with each assay.48 Two postharvest field seasons were examined in addition to the entries stored for 1 year. Entry × year interactions for iron bioavailability were not significant between the two postharvest sample sets and were combined into a single postharvest value. Statistical Analysis. All statistical analyses were conducted using SAS 9.2 (SAS Institute Inc., Cary, NC, USA). Mean separations for entries were determined using the Proc MIXED procedure with the model including entry (12 levels) and postharvest or storage treatment (2 levels) as fixed effects and field replicates (2 levels) as a random effect followed by a Tukey post hoc test. Pearson correlation coefficients were calculated to determine the associations between measured variables and cooking time for each field replicate across the four market classes. Differences with P values of ≤0.05 were considered statistically significant.
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RESULTS Cooking Times and Classifications of the HNP. Significant differences (P < 0.0001) in postharvest cooking times were observed across the HNP entries, with a minimum cooking time of 20 min for G23086 to a maximum of 68 min for PR0737-1 (Table 2). Entry × year interaction was not 8594
DOI: 10.1021/acs.jafc.6b03100 J. Agric. Food Chem. 2016, 64, 8592−8603
Article
Journal of Agricultural and Food Chemistry Table 2. Cooking Times and Classifications of the Health & Nutrition Panela cooking time (min) market class
entry
cooking class
postharvest
stored for 1 year
cooking increaseb
yellow
Cebo Cela Uyole 98 Canario
fast moderate slow
23 g 37 de 45 c
29 g 47 f 62 d
8 11 18
cranberry
G23086 OPS-RS4 Katarina Kibala
fast moderate slow
20 g 33 f 38 d
26 g 46 f 57 e
8 14 20
red mottled
JB178 Vazon-7 PR0737-1
fast moderate slow
35 ef 51 b 68 a
46 f 69 c 89 a
12 20 22
light red kidney
AC ELK Clouseau Pink Panther
fast moderate slow
34 ef 43 c 52 b
55 e 64 d 79 b
26 25 30
Values are presented as means of two field replicates per entry, measured in two postharvest field seasons (2012, 2013) and in seed stored for 1 year in ambient conditions. Means sharing the same letter in each column are not significantly different at P < 0.05. bMean difference in cooking time between seed from postharvest field season 2012 and seed stored for 1 year. a
Table 3. Nutrient Retention of Cooked Entries in the Health & Nutrition Panela retention after cookingb (%) postharvest
stored for 1 year
cooking class
starch
fiber
protein
ash
starch
fiber
protein
ash
yellow
Cebo Cela Uyole 98 Canario
fast moderate slow
98 ab 87 c 97 ab
88 abc 76 d 79 cd
89 abc 76 g 82 f
75 ab 59 def 64 de
99 a 89 b 90 ab
88 ab 71 c 75 c
89 a 71 f 78 de
73 a 53 c 59 bc
cranberry
G23086 OPS-RS4 Katarina Kibala
fast moderate slow
95 abc 91 abc 92 abc
74 cd 77 cd 79 bcd
90 ab 87 bcde 83 ef
71 bc 61 def 58 ef
93 ab 97 ab 90 ab
78 bc 77 bc 76 c
83 bc 77 de 76 e
66 ab 59 c 53 c
red mottled
JB178 Vazon-7 PR0737-1
fast moderate slow
96 abc 89 bc 94 abc
91 ab 87 abc 91 ab
89 abcd 78 g 85 def
74 ab 57 f 65 cd
93 ab 94 ab 94 ab
91 a 88 ab 91 a
84 bc 66 g 79 cde
69 a 54 c 59 bc
light red kidney
AC ELK Clouseau Pink Panther
fast moderate slow
99 a 95 abc 99 ab
96 a 82 bcd 98 a
92 a 89 ab 85 cdef
78 a 75 ab 65 cd
95 ab 92 ab 96 ab
88 ab 73 c 91 a
87 ab 81 cd 79 de
69 a 59 c 57 c
market class
entry
a Values are means of two field replicates for each entry, measured postharvest and after storage in ambient conditions for 1 year. Means sharing the same letter in each column are not significantly different at P < 0.05. bRetention values calculated by comparing content differences in 100 lyophilized raw and cooked whole seed.
Nutrient Retention in the HNP. Retention values for the major nutritional components of the seeds (starch, fiber, protein, ash) are shown in Table 3. Little variation in postharvest starch retention was detected among the different seed types of the HNP, with no discernible differences between the faster and slower cooking classes (Table 3). Postharvest fiber retentions varied significantly (P < 0.01) among the 12 HNP entries, but the amount of total dietary fiber retained after cooking was independent of cooking class (Table 3). Protein retention was significantly influenced by entry (P < 0.001) and ranged from 76% in Uyole 98 to 92% in AC ELK. Protein retention was associated with cooking class such that the faster cooking genotypes retained more protein (Table 3). Ash retention was also significantly influenced by entry (P < 0.0001), ranging from 57% in Vazon-7 to 78% in AC ELK. Compared to the slower cooking entries in each market class,
significant, and cooking time rank across the entries was similar between the two field seasons. The mean cooking time of the HNP entries increased 23−47% after the storage treatment, ranging from 26 min for the cranberry G23086 to 89 min for the red mottled PR0737-1 (Table 2). F tests for storage treatment (P < 0.0001) and entry × storage interaction (P < 0.0001) were significant. The cooking time response to storage was associated with seed type. Cooking times of yellow and red mottled entries increased 13:1), when considering earlier Caco-2 cell culture experiments documenting a maximal inhibition of FeCl3 uptake by phytate occurring at a molar ratio of 10:1.88 Yet, clear distinctions in iron uptake were demonstrated between the different market and cooking classes of the HNP. At this point, there is no clear explanation as to why higher iron uptake values were found in several HNP entries after storage (Table 8). The degradation of phytate, phenolic compounds, and fiber polymers could all be contributing to the release of iron from insoluble complexes during the storage process. Ironically, these are the same factors that are responsible for the physiochemical changes that lead to longer cooking times in dry beans.54 An opportunity arises from the demonstration that fastcooking dry beans (although dynamic among themselves) have more bioavailable iron when compared to their market class counterparts. The unique characteristics exhibited by the fastcooking entries of the HNP can be examined in better detail to determine which nutrient compositions, iron distribution patterns, and phenolic profiles are the most beneficial in promoting the absorption of iron. Once pin-pointed, these same phenotypes can be used by breeding programs to help identify positive or negative factors of iron absorption in the selection of new breeding lines. By examining the nutritional concentrations, contents, and densities of the cooked seed in the HNP (processed under defined cooking conditions and cooking times), the results of this study provide evidence to answer a fundamental questionbesides a reduction in cooking time, what other attributes does a fast-cooking dry bean offer as solutions aimed at effectively treating dietary nutrient deficiencies? The HNP model shows that a faster cooking, more nutritious, and more easily digested seed architecture could be traits that would improve the next generation of Andean dry beans. These traits would be especially valuable in varieties being developed for populations who rely on beans as a major source of protein and minerals. These traits also have value for consumers searching for nutritious foods that are convenient to prepare and easily incorporated into meals.
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Article
AUTHOR INFORMATION
Corresponding Author
*(K.A.C.) E-mail:
[email protected]. Phone: (517) 353-0210. Funding
This work was supported in part by funding from the Norman Borlaug Commemorative Research Initiative of the U.S. Agency for International Development, Project 021-22310-004-11R, and by the U.S. Department of Agriculture, Agricultural Research Service Projects 5050-21430-01000D (K.A.C.), 8062-52000-001-00-D (R.P.G.), and 58-6250-0-008 (M.A.G.). This work was also supported in part by PHS Grant R01CA172375 from the National Cancer Institute (H.J.T.). The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. government. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank Yasmin Salat, Mary Bodis, Yongpei Chang, and Dimas Echeverria for assistance with sample preparation and analyses.
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ABBREVIATIONS USED ADP, Andean diversity panel; HNP, Health & Nutrition Panel; LR, light red kidney; PA-P, phytic acid phosphorus REFERENCES
(1) Graham, P. Soil biology with an emphasis on symbiotic nitrogen fixation. In Nitrogen Fixation in Crop Production; Emerich, D., Krishnan, H., Eds.; Crop Science Society of America: Madison, WI, USA, 2009; pp 171−209. (2) Broughton, W.; Hernandez, G.; Blair, M.; Beebe, S.; Gepts, P.; Vanderleyden, J. Beans (Phaseolus spp.) − model food legumes. Plant Soil 2003, 252, 55−128. (3) Messina, V. Nutritional and health benefits of dried beans. Am. J. Clin. Nutr. 2014, 100, 437S−442S. (4) Bliss, F. A.; Brown, J. S. Breeding common bean for improved quantity and quality of seed protein. In Plant Breeding Reviews; Janick, J., Ed.; Springer: New York, 1983; pp 59−102. (5) de Jager, I. Literature Study: Nutritional Benefits of Legume Consumption at Household Level in Rural Areas of sub-Saharan Africa; Wageningen University: 2013; Vol. 53, pp 1−95, http://www. N2Africa.org. (6) Akibode, S.; Maredia, M. Global and Regional Trends in Production, Trade and Consumption of Food Legume Crops; Department of Agricultural, Food and Resource Economics, Michigan State University, 2011; p 87. (7) Beebe, S.; Gonzalez, A.; Rengifo, J. Research on trace minerals in the common bean. Food Nutr. Bull. 2000, 21, 387−391. (8) Petry, N.; Boy, E.; Wirth, J.; Hurrell, R. Review: The potential of the common bean (Phaseolus vulgaris) as a vehicle for iron biofortification. Nutrients 2015, 7, 1144−1173. (9) Beebe, S. Common bean breeding in the tropics. Plant Breed. Rev. 2012, 357−426. (10) Wessells, K. R.; Singh, G. M.; Brown, K. H. Estimating the global prevalence of inadequate zinc intake from national food balance sheets: effects of methodological assumptions. PLoS One 2012, 7, e50565. (11) McLean, E.; Cogswell, M.; Egli, I.; Wojdyla, D.; de Benoist, B. Worldwide prevalence of anaemia, WHO vitamin and mineral nutrition information system, 1993−2005. Public Health Nutr. 2009, 12, 444−454.
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.6b03100. Supplementary Table 1, seed mass retention values between the raw and cooked entries of the HNP, following harvest and after a year in storage. Supplementary Tables 2−7, concentration and content values for starch, fiber, protein, iron, zinc, and phytate in lyophilized raw/cooked seed. Supplementary Table 8, retention values for dietary minerals potassium, calcium, magnesium, iron, zinc, and copper. Supplementary Table 9, correlation coefficients and associated P values between cooking time, nutrient retention, and serving densities. Supplementary Table 10, correlations between the retention of phytate, protein, and minerals. Supplementary Table 11, phytate iron/zinc molar ratios of the 12 HNP entries (PDF) 8601
DOI: 10.1021/acs.jafc.6b03100 J. Agric. Food Chem. 2016, 64, 8592−8603
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