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Journal of Cereal Science xxx (2014) 1e6

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Journal of Cereal Science

journal homepage: www.elsevier .com/locate/ jcs

Use of wheat genetic resources to develop biofortified wheat withenhanced grain zinc and iron concentrations and desirable processingquality

Carlos Guzm�an a, Ana Sofía Medina-Larqu�e a, Govindan Velu a, *,Hector Gonz�alez-Santoyo a, Ravi P. Singh a, Julio Huerta-Espino b, Ivan Ortiz-Monasterio c,Roberto Javier Pe~na a

a Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), Apdo Postal 6-641, Mexico DF, Mexicob Campo Experimental Valle de Mexico INIFAP, Apdo. Postal 10, 56230 Chapingo, Edo de Mexico, Mexicoc Global Conservation Agriculture Program, International Maize and Wheat Improvement Center (CIMMYT), Apdo Postal 6-641, Mexico DF, Mexico

a r t i c l e i n f o

Article history:Received 21 May 2014Received in revised form21 July 2014Accepted 24 July 2014Available online xxx

Keywords:MalnutritionZincWheat qualityGenetic resources

Abbreviations: GH, Grain Hardness; GPRO%, GrainFlour Protein percentage; Fe, iron; LV, Loaf VolumeFSDS, Flour SDS Sedimentation; TW, Test Weight; Zn* Corresponding author. Tel.: þ52 5959521900x220

E-mail address: [email protected] (G. Velu).

http://dx.doi.org/10.1016/j.jcs.2014.07.0060733-5210/© 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Guzm�an, Ciron concentrations and desirable processin

a b s t r a c t

As a major cereal crop worldwide, wheat contributes on average one-fifth of the calories in the humandiet and is the main source of protein and nutrients for much of the world's population. Wheat va-rieties with improved nutritional quality, high grain yield and desirable processing quality attributesin adapted genetic backgrounds can help alleviate nutrient deficiencies among resource poor people.This paper reports advances in targeted crosses of landraces and ancestors of common wheat (Triticumaestivum L.), such as Aegilops tauschii, Triticum turgidum ssp. diccocoides, T. turgidum ssp. dicoccum andT. aestivum ssp. spelta species, which feature significant genetic variation for grain zinc and iron, withhigh-yielding bread wheat lines from the CIMMYT breeding program that have desirable processingand end-use quality. High-yielding lines that resulted from these crosses possessed preferred pro-cessing quality traits and 10e90% higher grain micronutrient concentrations than popular commercialvarieties.

© 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Micronutrient deficiency is one of the most important chal-lenges facing humanity. The lack of adequate levels of essentialvitamins and minerals (iron [Fe], zinc [Zn] and pro-vitamin A ca-rotenoids) affects more than 2 billion people (UNSCN, 2006).Pregnant women and young children are prone to acute micro-nutrient deficiency, which reduces physical and mental develop-ment in children below 5 years of age, and malnutrition isconsidered as the largest single contributor to disease in persons ofany age (UNSCN, 2006). Micronutrient deficiency is common indeveloping countries, where staple cereals (wheat, maize or rice)

Protein percentage; FPRO%,; M%TQ, Mixograph Torque;, zinc.0; fax: þ52 5558047558.

., et al., Use of wheat geneticg quality, Journal of Cereal Sc

providemost calories and diets are poor inmeat, poultry, fish, fruitsor vegetables (Bouis et al., 2011).

Plant breeding to develop biofortified crops with enhancedmicronutrient concentrations has emerged as a sustainable solu-tion to complement strategies such as supplementation or fortifi-cation, especially for micronutrient-deficient rural inhabitants withlimited access to formal markets or health care and who relyheavily on locally-grown staple food crops (Bouis et al., 2011).With the funding from the HarvestPlus Challenge Program and theCGIAR Research Program on Agriculture for Nutrition and Health,the International Maize and Wheat Improvement Center (CIMMYT,Int.) is leading a global effort to develop and disseminate to part-ners in South Asia high-yielding wheat varieties that contain highlevels of grain Zn concentration. South Asia suffers from highpopulation densities and alarming rates of malnutrition (Velu et al.,2012).

Breeding high-yielding, high-Fe and -Zn varieties requiressource materials that feature adequate genetic variation in con-centrations of those micronutrients. Screening studies have shownthat modern wheat cultivars are not a good source of genes to

resources to develop biofortified wheat with enhanced grain zinc andience (2014), http://dx.doi.org/10.1016/j.jcs.2014.07.006

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C. Guzm�an et al. / Journal of Cereal Science xxx (2014) 1e62

enhance the concentration of Zn and Fe (Ortiz-Monasterio andGraham, 2000; Zhao et al., 2009), probably because the breedingprograms in which they were developed focused on maximizingyield rather than improving nutritional quality. However, wheatlandraces and selected accessions of wheat ancestors such asAegilops tauschii, Triticum turgidum ssp. diccocoides, T. turgidumssp. dicoccum, and T. aestivum ssp. spelta do feature significantgenetic variation for grain Fe and Zn concentrations (Cakmak et al.,2004; Gomez-Becerra et al., 2009; Suchowilska and Wiwart,2012). Previous studies have explored the use of wide wheat ge-netic resources as sources of genes to enhance grain micronutrient(Fe and Zn) concentrations in adapted high-yielding backgrounds(Cakmak et al., 2000; Ficco et al., 2009; Morgounov et al., 2007;Zhao et al., 2009). Gomez-Becerra et al. (2010) identified morethan 200 Triticum spelta genotypes with Fe and Zn concentrationshigher than 50 mg/kg; Ortiz-Monasterio and Graham (2000)showed several accessions of Triticum dicoccum and Mexicanlandraces with superior concentrations for both micronutrientsand Chhuneja et al. (2006) reported Ae. tauschii and synthetic lineswith concentrations higher than 60 mg/kg for Fe and Zn. Theavailability in the primary and secondary wheat gene pools ofgenotypes containing high concentrations of micronutrients invarious studies were reported in Velu et al. (2014). The primarydriver for adoption of biofortified wheat varieties in small-holderfarmers must be superior yields, resistance to important diseasesand tolerance to heat, drought and potentially to micronutrient-deficient soils (Welch and Graham, 2004). This has been thestrategy of CIMMYT's Global Wheat Program. Specifically, severalsynthetic wheat lines generated from selected T. dicoccum, Triti-cum durum and Ae. tauschii accessions, as well as selected speltwheats and wheat landraces, have been crossed with high-yielding, elite bread wheats to develop high-yielding lines thatalso possess enhanced grain micronutrient concentrations, withhigher Zn content as a primary target trait. To obtain varietiesacceptable to farmers and which are commercially com-petitivedthat is, acceptable to millers, manufacturers and con-sumersdrigorous selection pressure was applied for grain yieldpotential, disease resistance, heat and drought tolerance andacceptable processing quality. For instance in South Asia whereChapatti is the main local unleavened flat bread, biofortified wheatproducts should have medium-to-hard grain texture, as well asextensible and medium-strength gluten, to produce flat breadwith acceptable (long-lasting) textural characteristics. Linesshowing superior dough extensibility combined with medium-to-high gluten strength can also be used for products such as yeast-leavened bread, thereby promoting small-to-intermediate-scalelocal industry. Several studies have concluded that wild relativesand synthetic hexaploids have greater allelic variation for gluteninsubunits than cultivated wheat and these alien genes offers po-tential means of expanding allelic variants controlling proteinswith desirable end-use quality (Lagudah and Halloran, 1988;William et al., 1993). A strong positive correlation between grainZn and protein content was shown in several studies (Feil andFossati, 1995; Morgounov et al., 2007; Peterson et al., 1986) sug-gesting that breeding for high Zn concentration may not affectprocessing and end-use quality. Conversely, Morgounov et al.(2007) reported a significant negative correlation between glu-tenin content and Zn and Fe concentrations among central Asianwheat varieties; however, more studies are needed to define thisrelationship in CIMMYT spring wheat germplasm.

The objectives of this study were to characterize 141 biofortifiedwheat lines with enhanced grain Zn and Fe concentrations for theirprocessing and end-use quality traits and to determine whetherthis breeding material has processing quality suitable to producedifferent end-use products.

Please cite this article in press as: Guzm�an, C., et al., Use of wheat geneticiron concentrations and desirable processing quality, Journal of Cereal Sc

2. Materials and methods

2.1. Plant material

We used grain samples of 141 advanced lines from the Har-vestPlus Yield Trial (HPYT) grown during the 2009e10 crop seasonin Ciudad Obreg�on, Sonora, M�exico, under full irrigated conditions.This is an optimally irrigated highly productive environment wherewheat grows in average temperature of 22 �C and matures with theincreased summer temperature (37 �C). The weather conditionsduring the 2009e2010 crop growing season was normal with theminimum temperature varied from 1 �C to 18 �C and maximumtemperature ranged between 16 �C and 38 �C. Trial entries wereevaluated following an alpha-lattice design with three replications.The basal dose of 50 kg nitrogen ha�1 and 40 kg phosphorus ha�1

was applied at the time of sowing and additional 100 kg N ha�1 wasapplied at the time of 2nd irrigation. Necessary agronomic practiceswere followed to raise a good crop. Plots were harvested at physi-ological maturity. The advanced lines were divided into five groupsdepending on their origin or cross: Ie 22modern breadwheat linesused as checks in this study; II e 35 lines resulting from the cross ofMexican landraces with modern cultivars; III e 26 lines derivedfrom the cross of spelt accessions with modern cultivars; IV e 45lines resulting from the cross of synthetic wheat lines (T. dicoccumaccessions � Ae. tauschii) with modern cultivars; and V e 13 linesderived from the cross of synthetic wheat lines (T. durumaccessions � Ae. tauschii) with modern cultivars. The completepedigree of each line is shown in Supplementary Material 1.

2.2. Statistical analysis

Statistical analyses were performed using Proc. Mixed in SAS 9.2version for Alpha-Lattice experimental design and standard devi-ation and phenotypic correlations were estimated.

2.3. Grain and rheological analyses

Grain Fe and Zn concentrations (mg/kg) were measured using abench-top, non-destructive, energy-dispersive X-ray fluorescencespectrometry (EDXRF) instrument (model X-Supreme 8000, OxfordInstruments plc, Abingdon, UK), previously standardized for high-throughput screening of Zn and Fe in whole wheat grain(Paltridge et al., 2012). Grain hardness (GH), grain protein (GPRO%)and moisture content were determined using near-infrared spec-troscopy (NIRS, NIR Systems 6500, Foss Denmark) according to theofficial method AACC 39-70A (AACC, 2000). Lower hardness index(%) values correspond to harder grains. Grain samples were milledusing Brabender Quadrumat Jr. (C.W. Brabender OHG, Germany).Flour protein (FPRO%) and moisture content were determined byNIRS (Foss NIR systems INFRATEC 1255, FOSS-TECATOR, Denmark).Both devices were calibrated based on AACCmethods (AACC, 2000)for moisture (AACCMethod 44-15A) and protein (AACCMethod 46-11A). Grain protein and flour protein were adjusted to a 12.5% and14% moisture basis, respectively. The SDS sedimentation test wasconducted using 1 g of flour, as described in Pe~na et al. (1990)recording volume in ml of sediment (FSDS). Dough developmentproperties were determined by computerized Swanson Mixograph(National Mfg., USA) using 35 g of flour, according to AACC method54-40A (AACC, 2000). Two parameters were obtained: doughdevelopment time (MDDT) and % torque*min (M%TQ). The strength(ALVW) and extensibility properties (tenacity/extensibility ratio,ALVP/L) were determined in the Chopin Alveograph (Trippette andRenaud, France), using 60 g flour samples and variable water ab-sorption (60e62%), based on solvent retention capacity. The bread-making test was carried out using 100 g flour according to the AACC


Table 1Average, standard deviation, maximum and minimum values for micronutrients and quality parameters for 5 different groups.

Group I (bread wheat checks) Group II (landrace origin) Group III (spelt origin) Group IV (emmer synthetic origin) Group V (durum synthetic origin)

Zn 21.7 ± 2.0 (15.8e24.3) 27.1 ± 10.3 (19.0e53.0) 30.1 ± 7.5 (14.1e44.4) 29.8 ± 7.2 (17.7e45.5) 25.8 ± 6.0 (19.6e36.7)Fe 29.4 ± 3.3 (23.9e35.9) 27.0 ± 1.5 (24.1e31.3) 31.9 ± 3.3 (22.9e38.6) 32.8 ± 2.9 (26.9e38.1) 28.8 ± 3.0 (24.1e33.6)TW 81.3 ± 1.0 (78.9e82.8) 76.4 ± 2.0 (75.0e82.2) 80.9 ± 2.2 (74.1e84.9) 81.4 ± 1.4 (78.3e83.9) 80.0 ± 1.1 (79.0e83.0)GH 41.6 ± 2.6 (36.4e46.6) 61.7 ± 7.7 (40.7e68.9) 44.5 ± 4.0 (37.3e57.1) 43.2 ± 3.5 (34.4e50.9) 44.7 ± 2.5 (41.0e49.4)GPRO% 13.0 ± 1.1 (11.1e15.0) 13.2 ± 0.4 (12.3e14.3) 13.4 ± 0.8 (11.6e15.0) 13.4 ± 0.9 (12.0e15.5) 13.6 ± 0.8 (12.3e15.0)FPRO% 11.9 ± 1.1 (10.2e14.0) 12.0 ± 0.5 (10.0e12.7) 12.3 ± 0.9 (10.7e13.9) 12.2 ± 1.1 (10.3e15.2) 12.5 ± 0.5 (11.9e13.5)FSDS 21.3 ± 1.0 (18.8e22.8) 21.1 ± 3.5 (10.3e23.5) 21.6 ± 1.4 (19.0e24.3) 20.9 ± 2.2 (13.3e23.5) 22.1 ± 0.6 (21.3e23.3)MDDT 2.7 ± 0.5 (1.5e3.6) 1.5 ± 0.3 (0.9e2.5) 2.5 ± 0.6 (1.6e3.9) 2.4 ± 0.7 (1.3e3.9) 2.3 ± 0.7 (1.6e3.8)M%TQ 108.6 ± 21.1 (67.9e152.3) 52.1 ± 9.0 (28.4e69.8) 103.6 ± 23.7 (65.2e151.4) 100.9 ± 33.8 (45.1e156.7) 91.8 ± 29.5 (60.0e150.0)ALVW 282.6 ± 83.6 (135e431) 110.9 ± 42.2 (37e253) 298.3 ± 99.0 (126e515) 290.9 ± 126.0 (88e599) 270.4 ± 142.2 (151e549)ALVPL 1.0 ± 0.3 (0.5e1.5) 0.6 ± 0.3 (0.3e1.8) 0.9 ± 0.2 (0.5e1.2) 0.9 ± 0.2 (0.5e1.5) 0.9 ± 0.5 (0.4e2.1)LV 775 ± 57.5 (670e900) 698.9 ± 42.9 (495e745) 802.5 ± 56.47 (660e920) 788.4 ± 66.8 (650e930) 777.3 ± 64.5 (685e910)

C. Guzm�an et al. / Journal of Cereal Science xxx (2014) 1e6 3

10-09 method (AACC, 2000) and bread loaf volume (LV) recorded.All data are given in Supplementary Material 1.

3. Results

3.1. Fe and Zn concentration

The average grain Fe and Zn concentration in check varieties(Group I) was 29.4 mg/kg and 21.7 mg/kg, respectively (Table 1).The maximum micronutrient concentration in this group was36 mg/kg Fe (GID 5996190) and 24 mg/kg for Zn (GID 5994262).Group II had several entries with higher Zn and Fe grain concen-trations than the highest levels found in group I (Figs. 1 and 2). Ingroups III and IV, lines with spelt and emmer synthetics origins,respectively, showed higher mean values for Zn and Fe than thoseof the checks and in each of these groups at least one linewas foundto have higher Fe and Zn values than the maximum value found ingroup I. In group III and IV, highest Zn levels were 44 mg/kg (GID6181266) and 45 mg/kg (GID 618149), respectively. In all groups

Fig. 1. Distribution of wheat lines for grain Zn (a) and Fe (b) concentration for each ofthe five groups.


there were lines with significantly higher Zn values than themaximum for the checks (Fig.1). For grain Fe content, groups III andIV showed the highest number of lines with high concentrations,while groups II and V did not show promising results compared tothe checks (Fig. 1). For grain Zn concentration, groups IIeV hadmore lines with high Zn than group I. Remarkably, some genotypesin groups II, III and IV had very high Zn concentrations (up to 53mg/kg) and therewere lines with 53, 44 and 44.5mg/kg (in groups II, IIIand IV, respectively), which is more than twice the grain Zn levelsof the best commercial varieties (Fig. 3).

Using group I micronutrient content averages (29.4 and 21.7mg/kg for Fe and Zn, respectively) as a reference, groups III and IV hadthe highest proportion of lines with superior micronutrient con-centrations (Fig. 2).

3.2. Grain physical and chemical characteristics

Grain samples were tested for different processing quality traits,including the morphological index of the grain Test Weight (TW).

Fig. 2. Frequency distribution of grain Zn (a) and Fe (b) concentrations in each of thefive groups.


Fig. 3. Percentage of wheat lines in groups IIeV showing higher Fe and Zn concentrations than the average of the checks (group I).


Group I had the highest TW values (average of 81.34 kg/hl), whichindicates the presence of plump grain in trials conducted underoptimum conditions. All other groups except II also had an averageTWover 80 kg/hl, with well filled grains. Group II lines weremostlyderivatives of Mexican landraces and showed the lowest averageTW value (76.37 kg/hl), which could be due to having smaller orslightly shriveled grains, or lacking adaptation to the warm, irri-gated, high-production environment of Ciudad Obreg�on. Fortexture, groups I, III, IV and V had similar average grain hardnessvalues, although there was considerable variation for hardnesswithin each groups, with phenotypes showing a range of valuesfrom hard to soft grains. Group II comprised mainly soft grain lines,with only five lines showing hard or semi-hard texture.

No significant differenceswere found formean GPRO% and FPRO% among the groups. The differences between the minimum andmaximum values in all the groups were around 4%. Significantpositive correlations were found between GPRO% and Fe in groups

Fig. 4. Percentage of wheat lines in each of the five groups showing extensible,balanced or tenacious gluten, based on alveograph P/L ratio.


I, and V, but only between GPRO% and Zn in group I (r ¼ 0.44;P < 0.05).

3.3. Rheological and end-use properties

The FSDS volume provides a rough estimate of gluten strength.On average, all groups showed high FSDS values, although groups IIand IV had some lines with low values. Performance in the mixo-graph was heterogeneous, with lines in each group showingacceptable values for dough development time (MDDT) and doughstrength (M%TQ), while others showed very weak strength,considered insufficient for yeast-leavened bread or even unleav-ened flat breads. These results were confirmed with the alveograph(ALVW), which gives a more rigorous measure of dough strengthand correlates closely with M%TQ (in this study: r ¼ 0.87;P < 0.001). As for M%TQ, the average ALVW value in each group wasacceptable for bread making, with the exception of group II, inwhich gluten strength (ALVW) was very low. Dough extensibility(ALVP/L) was generally good in most lines of all groups, with a fewexceptions (ALVP/L � 1.4) that would not be suitable for breadmaking. Group II had the most lines with moderate-to-highextensibility. In groups I, III and IV most lines had balancedgluten (ALVP/L 0.8e1.3), whereas in group Vmore lines showed lowextensibility (Fig. 4). The bread-making test revealed acceptableaverage bread loaf volumes for all groups except II, most of whoselines would result in bread making leavened bread products ofinferior quality and perhaps unleavened breads with poor retentionof freshness after baking. Medium-to-high loaf volumesda fewexceeding 900 mldresulted from most lines in the other groups,with a few exceptions.

Each line was then classified into one of five end-use qualitytypes established in the CIMMYT Wheat Chemistry and QualityLaboratory by Pe~na (2011, unpublished document), based on rangeof values for GH, GPRO%, FPRO%, MDDT, ALVPL, and ALVW: use-type1, Pan type breads (mechanized industry); 2, leavened breads(semi-mechanized industry), flat breads, dry and fresh noodles andsteam breads; 3, dense breads, flat breads (handmade); 4, steambread, white-salted noodles and biscuits; and 5, utility wheat (poorquality). Only a few lines were included in the quality type 5. Thegroups III and IV were predominated by lines with quality types 1and 2, which is linked to mediumehigh strength and good


C. Guzm�an et al. / Journal of Cereal Science xxx (2014) 1e6 5

extensibility; in group V, most of the lines were classified in type 3,due to the prevalence of medium strong and extensible gluten; andin group II, most of the lines fall in the type 4, generally good forbiscuit making, due to their soft texture and weak and extensiblegluten.

3.4. Micronutrients concentration vs. end-use quality

To combine high micronutrient concentration and acceptableprocessing quality in adapted genetic backgrounds, we examinedboth traits together for each group. Group II did not show a sig-nificant increment in grain Fe concentration compared to thechecks, but there was a strong increase for Zn concentration in tenlines compared to the checks. Of these ten lines only two showedslightly enhanced Fe concentration compared to the average valuefor the checks (29.4 mg/kg). One of these lines showed poorextensibility and was classified as quality type 5. The other one,showed excellent extensibility, weak gluten (ALVW ¼ 94) and softtexture, and therefore had all the characteristics required to be agood biscuit making wheat cultivar. In group III, 11 lines showedsignificantly enhanced concentrations for both micronutrients (atleast 10% more Fe and at least 20% more Zn). Three of these linesbelong to quality type 1 (mechanized bread making, good exten-sibility and high gluten strength), six were quality type 2 (flatbreads, good extensibility and mediumehigh gluten strength), onewas quality type 3 (handmade bread) and another one was qualitytype 4 (biscuits, soft texture with weak and extensible gluten). Ingroup IV,19 lineswith significantly higher Fe and Zn concentrationswere divided into quality types 1¼8 lines, type 2¼ 5 lines and type3 ¼ 6 lines. Lastly, group V, with three lines showing significantlyincreased micronutrient concentrations, of which two of thembelonged to quality type 1 and the other belongs to quality type 3.

4. Discussion

Considering the substantial genetic diversity that exists for Znand Fe, CIMMYT followed the strategy of crossing selected geneticresources and synthetic lines showing high levels of micronutrientswith high-yielding modern wheat lines to develop biofortifiedwheat derivatives with the preferred agronomic features. In thisstudy, the advanced breeding lines resulting from this process wereanalyzed for micronutrient concentrations and also for processingquality traits. Ensuring acceptable processing quality would satisfyneeds of target population in rural and urban areas as the bio-fortified wheat varieties must have the requirements of the con-sumer (baking quality, taste and keeping properties) and wholevalue chain (farmers, millers, manufacturers, and consumers).

Although grain Fe concentration is an important trait for Har-vestPlus project, Zn concentration has received special attentionbecause more than 26% of the target population in South Asiasuffers from Zn deficiency. That probably explains why most linesin this study showed significantly greater grain Zn concentrationsthan the check varieties, as well as the practice of choosing parentswith high Zn and applying greater selection pressure for Zn con-centration in breeding, based on various study results suggestingthat higher Zn is positively associated with higher Fe concentration(Gomez-Becerra et al., 2010; Morgounov et al., 2007; Zhao et al.,2009). In our study, positive significant correlation was observedbetween Fe and Zn across five groups (r ¼ 0.37; P < 0.01). Apartfrom this general trend, several linesdparticularly from groups IIIand IVdhadmicronutrient concentrations significantly higher thanthose of the checks, confirming the excellence of T. spelta andT. dicoccum synthetic derivatives as sources of genes for highermicronutrient concentrations as Gomez-Becerra et al. (2010) andOrtiz-Monasterio and Graham (2000) reported previously.


Although several landraces, spelt and even synthetic lines haveshown good performances in quality analysis (Ali et al., 2013;Konvalina et al., 2013; Mondini et al., 2014), other studies havereported that those materials, as any others, can have great dif-ferences in quality traits, and some of them be completely unsat-isfactory for the development of different wheat products(Lagudah et al., 1987; Mikos and Podolska, 2012; Wilson et al.,2008). Strikingly, a large proportion of lines in this studypossessed very good quality traits, with most showing goodextensibility, a key end-use quality parameter in manufacturingany wheat product. This is probably due to the use of modern lineswith good-to-excellent quality as background parents in thecrosses with high Zn and Fe donors, and often using 1 or 2 back-crosses or three-way crosses with the adapted good quality par-ents in the breeding process. Although this study was conducted ina single environment, the environment of Ciudad Obregon, Mexicois representative of many of the high-yielding environmentsworldwide and there is an established history of breeding linesfrom Obregon being well adapted in these target environments(Braun et al., 2010). Large scale multi-location testing of bio-fortified high Zn wheat lines in target environments revealedGenotype � Environment interaction is not a serious issue due tointermediate to high heritability for grain Zn and Fe and otherquality traits (Velu et al., 2012).

Gluten strength differed among the groups. In group II, weakgluten lines predominated but most were very extensible. This islinked to their soft texture and makes them good candidates forbiscuit production. In this group, the use of Mexican landracesthat are known to possess soft grain texture (Ayala et al., 2013)could have led to selection of the soft grain trait in derived lines.Soft grain texture is not common in CIMMYT improved wheatgermplasm. In groups III and IV, medium-strong and stronggluten lines were the most numerous, which is linked to theoverall good extensibility of the lines and makes them highlyacceptable for homemade unleavened flat breads, such as cha-patti, or leavened breads in mechanized or semi-mechanizedlocal industry of South Asia. In these groups, the large numberof lines with high micronutrient concentrations made it easy tofind lines combining high Fe and Zn with good end-use quality.Finally, group V lines generally had slightly lower gluten quality,although they could be used as a progenitor to enhance micro-nutrient concentrations.

5. Conclusions

The advanced breeding lines analyzed from the HarvestPlusyield trial showed good processing quality characteristics and asignificant enhancement in grain Zn and Fe concentrations, espe-cially those originating from spelt and emmer synthetic back-grounds. Our results show that there has been progress indeveloping varieties that possess high Zn levels and desirableprocessing quality, as well as high yield potential, even though theZn and Fe donor sources are wild relatives and landraces. This wasachieved by considering processing quality and yield-related traitswhen designing the crosses and by applying selection pressure forvarious quality characteristics in the breeding lines. The final re-leases of biofortified wheat varieties in the target regions will helpimprove the livelihoods and health of numerous resource-poor,micronutrient-deficient people, as well as offer new biofortifiedvarieties acceptable by the whole wheat value chain.

Acknowledgments

We greatly appreciate financial support from the HarvestPluschallenge program of CGIAR consortium and special thanks to Mike



Listman for editing and improving the English language of thispaper.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jcs.2014.07.006.

References

AACC International, 2000. Approved Methods of the American Association of CerealChemists, 10th ed. AACC International, St. Paul, MN, USA.

Ali, A., Arshad, M., Mastrangelo, A.M., De Vita, P., Gul-Kazi, A., Mujeeb-Kazi, A., 2013.Comparative assessment of glutenin composition and its relationship withgrain quality traits in bread wheat and synthetic derivates. Pak. J. Bot. 45,289e296.

Ayala, M., Guzm�an, C., Alvarez, J., Pe~na, R.J., 2013. Characterization of genetic di-versity of puroindoline genes in Mexican wheat landraces. Euphytica 53e63.

Bouis, H.E., Hotz, C., McClafferty, B., Meenakshi, J.V., Pfeiffer, W.H., 2011. Bio-fortification: a new tool to reduce micronutrient malnutrition. Food Nutr. Bull.32, 31Se40S.

Braun, H.J., Atlin, G., Payne, T., 2010. Multi-location testing as a tool to identify plantresponse to global climate change. In: Reynolds, M.P. (Ed.), Climate Change andCrop Production. CABI press, Oxford, UK, pp. 115e138.

Cakmak, I., Ozkan, H., Braun, H., Welch, R., Romheld, V., 2000. Zinc and iron con-centrations in seeds of wild, primitive, and modern wheats. Food Nutr. Bull. 21,401e403.

Cakmak, I., Torun, A., Millet, E., Feldman, M., Fahima, T., Korol, A., Nevo, E., Braun, H.,Ozkan, H., 2004. Triticum dicoccoides: an important genetic resource forincreasing Zinc and Iron concentration in modern cultivated wheat. Jpn. Soc.Soil Sci. Plant Nutr. 50, 1047e1054.

Chhuneja, P., Dhaliwal, H.S., Bains, N.S., Singh, K., 2006. Aegilops kotschyi andAegilops tauschii as sources for higher levels of grain Iron and Zinc. Plant Breed.531, 529e531.

Ficco, D.B.M., Riefolo, C., Nicastro, G., De Simone, V., Di Gesù, a. M., Beleggia, R.,Platani, C., Cattivelli, L., De Vita, P., 2009. Phytate and mineral elements con-centration in a collection of Italian durum wheat cultivars. Field Crops Res. 111,235e242.

Feil, B., Fossati, D., 1995. Minerals composition of Triticale grains as related to grainyield and grain protein. Crop Sci. 35, 1426e1431.

Gomez-Becerra, H.F., Yazici, A., Ozturk, L., Budak, H., Peleg, Z., Morgounov, A.,Fahima, T., Saranga, Y., Cakmak, I., 2009. Genetic variation and environmentalstability of grain mineral nutrient concentrations in Triticum dicoccoides underfive environments. Euphytica 171, 39e52.

Gomez-Becerra, H.F., Erdem, H., Yazici, a., Tutus, Y., Torun, B., Ozturk, L., Cakmak, I.,2010. Grain concentrations of protein and mineral nutrients in a large collectionof spelt wheat grown under different environments. J. Cereal Sci. 52, 342e349.

Konvalina, P., Sterba, Z., Capouchova, I., Moudry, J., Moudry Jr., J., 2013. Bakingquality of genetics resources of spring forms of Triticum spelta L. J. Food Agric.Environ. 11, 475e476.


Lagudah, E.S., Halloran, G.M., 1988. Phylogenetic relationships of Triticum tauschiithe D genome donor to hexaploid wheat. I. Variations in HMW subunits ofglutenin and gliadins. Theor. Appl. Genet. 75, 592e598.

Lagudah, E.S., Macritchie, F., Halloran, G.M., 1987. The influence of high-molecular-weight subunits of glutenin from Triticum tauschii on flour quality of synthetichexaploid wheat. J. Cereal Sci. 5, 129e138.

Mikos, M., Podolska, G., 2012. Bread-making quality of old common bread (Triticumaestivum ssp. vulgare L.) and spelt (Triticum aestivum ssp. spelta L.) wheat cul-tivars. J. Food Agric. Environ. 10, 221e224.

Mondini, L., Grausgruber, H., Pagnotta, M.A., 2014. Evaluation of European emmerwheat germplasm for agro-morphological, grain quality traits and moleculartraits. Genet. Resour. Crop Evol. 61, 69e87.

Morgounov, A., G�omez-Becerra, H.F., Abugalieva, A., Dzhunusova, M.,Yessimbekova, M., Muminjanov, H., Zelenskiy, Y., Ozturk, L., Cakmak, I., 2007.Iron and zinc grain density in common wheat grown in Central Asia. Euphytica155, 193e203.

Ortiz-Monasterio, I., Graham, R., 2000. Breeding for trace minerals in wheat. FoodNutr. Bull. 21, 392e396.

Paltridge, N.G., Milham, P.J., Ortiz-Monasterio, J.I., Velu, G., Yasmin, Z., Palmer, L.J.,Guild, G.E., Stangoulis, J.C.R., 2012. Energy-dispersive X-ray fluorescence spec-trometry as a tool for zinc, iron and selenium analysis in whole grain wheat.Plant Soil 361, 251e260.

Pe~na, R.J., Amaya, A., Rajaram, S., Mujeeb-Kazi, A., 1990. Variation in quality char-acteristics associated with some spring 1B/1R translocationwheats. J. Cereal Sci.12, 105e112.

Peterson, C.J., Johnson, V.A., Mattern, P.J., 1986. Influence of cultivar and environ-ment on mineral and protein concentrations of wheat flour, bran, and grain.Cereal Chem. 63, 183e186.

Suchowilska, E., Wiwart, M., 2012. A comparison of macro-and microelementconcentrations in the whole grain of four Triticum species. Plant Soil Environ.141e147.

UNSCN, 2006. Double burden of malnutrition: a common agenda. In: 33rd AnnualSession of United Nations Standing Committee on Nutrition, Geneva,Switzerland.

Velu, G., Ortiz-Monasterio, I., Cakmak, I., Hao, Y., Singh, R.P., 2014. Biofortificationstrategies to increase grain zinc and iron concentrations in wheat. J. Cereal Sci.59, 365e372.

Velu, G., Singh, R.P., Huerta-Espino, J., Pe~na-Bautista, R.J., Arun, B., Mahendru-Singh, A., Yaqub Mujahid, M., Sohu, V.S., Mavi, G.S., Crossa, J., Alvarado, G.,Joshi, A.K., Pfeiffer, W.H., 2012. Performance of biofortified spring wheat ge-notypes in target environments for grain zinc and iron concentrations. FieldCrops Res. 137, 261e267.

Welch, R.M., Graham, R.D., 2004. Breeding for micronutrients in staple food cropsfrom a human nutrition perspective. J. Exp. Bot. 55, 353e364.

William, M.D.H.M., Pe~na, R.J., Mujeeb-Kaz, A., 1993. Seed protein and isozymevariations in Triticum tauschii (Aegilops squarrosa). Theor. Appl. Genet. 87,257e263.

Wilson, J., Bechtel, D., Wilson, G., Seib, P., 2008. Bread quality of spelt wheat and itsstarch. Cereal Chem. 85, 629e638.

Zhao, F.J., Su, Y.H., Dunham, S.J., Rakszegi, M., Bedo, Z., McGrath, S.P., Shewry, P.R.,2009. Variation in mineral micronutrient concentrations in grain of wheat linesof diverse origin. J. Cereal Sci. 49, 290e295.




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use of wheat genetic resources to develop biofortified wheat with enhanced grain zinc and iron...

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