Development of a core collection of Triticum and Aegilops species for improvement of wheat for activity against chronic diseases

  • Meenakshi Santra1,

    Affiliated with

    • Shawna B Matthews1 and

      Affiliated with

      • Henry J Thompson1Email author

        Affiliated with

        Agriculture & Food Security20132:4

        DOI: 10.1186/2048-7010-2-4

        Received: 26 September 2012

        Accepted: 29 January 2013

        Published: 15 February 2013

        Abstract

        Background

        The objective of this study was to develop a core collection of Triticum and Aegilops species as a resource for the identification and characterization of wheat lines with preventive activity against chronic diseases. Given that cancer is the leading cause of mortality in the world and shares risk factors with obesity, type-2 diabetes, and cardiovascular disease, and given that wheat has been reported to protect against these diseases, the core collection was developed based on cancer prevalence.

        Methods

        The Germplasm Resources Information Network (GRIN) database was used to identify Triticum and Aegilops species grown in regions of the world that vary in cancer prevalence based on the International Agency for Cancer Research GLOBOCAN world map of cancer statistics (2008). Cancer incidence data drove variety selection with secondary consideration of ploidy, center of origin, and climate.

        Results

        Analysis indicated that the geographic regions from which wheat is considered to have originated have a lower incidence of cancer than other geographic regions (P <0.01), so wheat lines from countries that comprise the ‘Fertile Crescent’ were highly represented in the core collection. A total of 188 lines were selected from 62,571 accessions maintained by GRIN. The accessions identified comprised two genera and 14 taxa of 10 species within 19 groups from 82 countries. The core collection is comprised of 153 spring, 25 winter, and five facultative selections of wheat.

        Conclusions

        A diverse core collection of wheat germplasm has been established from a range of regions worldwide. This core collection will be used to identify wheat lines with activity against chronic diseases using anticancer activity as a screening tool.

        Keywords

        Aegilops Anticancer activity Cancer Core collection Triticum Wheat germplasm

        Background

        The consumption of whole grains has long been associated with a healthy lifestyle and chronic disease prevention; in particular, multiple studies have correlated whole-wheat consumption with protection against chronic diseases including cardiovascular disease, stroke, type 2 diabetes, and cancer at multiple sites [18]. However, these studies have failed to discriminate between the type of wheat that is consumed and the chronic disease protective effect observed. Specifically, the USDA has germplasm from 62,571 distinct wheat varieties; given the well-described differences in agronomic traits as a result of genetic polymorphisms within wheat species, as well as the recently characterized metabolite differences between and within wheat species and subspecies [9], further investigation of the chronic disease preventive capacity of individual wheat varieties is required.

        In this paper, we propose that a neglected opportunity in the field of diet and chronic disease prevention is the use of staple food crops with defined bioactivity for daily consumption [10]. The rationale underlying this approach recognizes that societies have chosen their staple food crops, which are affordable and generally available to all individuals across socioeconomic strata, and that societies willingly consume these staples in large quantities on a daily basis. These consumption patterns thus provide a stable flow of health beneficial phytochemicals in much the same way that an oral drug is taken to maintain plasma concentrations of the active ingredient in a beneficial range [11]. Further research on bioactivity of specific varieties of these staple food crops is critical, given that major chronic diseases, including obesity, type-2 diabetes, cardiovascular disease, stroke, and cancer, account for over 60% of deaths worldwide [12, 13], are interrelated at the molecular and cellular levels and share many common risk factors [1416], and, most importantly, are also considered preventable through lifestyle choices of which diet is considered to play a prominent role [1719].

        While concern exists that the genetic factors driving the occurrence and progression of cancer and other chronic diseases are so powerful that diet can have little impact, most evidence indicates that the key strategy to conquering chronic diseases like cancer is through prevention particularly when the prevention strategy is routinized from ‘womb to tomb’ (reviewed in [20]). However, in addition to the general presumption that all varieties of a particular staple food crop are created equal with respect to health benefits, one of the challenges of this approach is the assumption that the ingredients which a food is processed into, rather than the food itself, is the most critical factor accounting for health benefits [10]. The work reported in this paper was initiated to provide a resource for evaluating the first premise, that is, that all botanically defined lines of wheat (Triticum and Aegilops species) have equivalent chronic disease fighting activity with anticancer activity providing a focal point for analysis. Cancer was chosen because among these chronic diseases, the prevalence of cancer continues to increase globally and cancer is now the leading cause of chronic disease related mortality in the world [21]; furthermore previously published reports have described an inverse association between wheat consumption and cancer incidence.

        Wheat is ranked second, after rice, among all members of the Poaceae family in terms of the amount consumed by the global population [22]. Wheat is used in the preparation of a wide variety of foods for everyday use, including bread, pasta/macaroni/noodles, bulgur, cookies, biscuits, cakes, cereals, pizza, vermicelli, couscous, pastry, and chapatti/flatbread [23, 24]. It is also fermented to make beer and other alcoholic beverages. Wheat’s role as a primary human dietary component is due to its large grain size, agronomic adaptability, ease of storage, and nutritional quality. While a limited number of wheat lines account for most of wheat products consumed globally due to the emergence of global industrial food systems, some ancient wheat lines- such as einkorn and emmer- are still consumed as cereal substitutes in Middle Eastern countries, where wheat is considered to have originated [25]. These grains are very small and difficult to harvest and clean. As such, they are often used in porridge or soup without grinding or processing. In the Arab world (including Iraq, Syria, and Tunisia), soft green (immature) wheat grains, mostly domesticated tetraploid emmer, are sundried and roasted to make a food called Freekeh. In addition, people in Arab countries routinely mix Freekeh made from domesticated landraces of wheat grains with meat and spices in their daily foods.

        As noted above, wheat is consumed in large amounts worldwide, but the type of wheat and the manner in which it is consumed differ markedly depending on geographic region. Because of the novel events underlying the domestication of wheat, there are major genetic differences among the types of wheat commonly consumed. As a result of this inherent diversity, the Germplasm Resources Information Network (GRIN) has accumulated over 62,571 wheat-related accessions [26]. The general approach to working with such a large resource is to devise a strategy by which to pick a representative sample of lines from the total resource (collection) that is small enough to manage for use in research yet large enough to capture the diversity of the population for the trait(s) of interest. The resulting subsample of germplasm is referred to as a core collection [27]. Herein, a core collection of wheat lines for future use in chronic disease prevention research is described.

        Methods

        Source of plant materials

        The Triticum and Aegilops collections at GRIN (USDA/ARS, Aberdeen, Idaho) include 59,564 and 2,650 accessions, respectively [26]. Only Triticum and Aegilops were selected for establishing this core collection with the reasoning that these two genera comprise the majority of wheat lines that have emerged due to domestication through natural selection and polyploidization. The accessions chosen for inclusion in the core collection are described in Table 1. All available information was obtained on selected accessions, including passport information, characterization, and evaluation.
        Table 1

        A summary of the Triticum and Aegilops species used for core collection

        Species

        Genome

        Total active accessions at GRIN

        Total number in core collection

        Base species (%)

        Aegilops speltoides var. speltoides

        BB/GG

        9

        3

        33.33

        Aegilops speltoides var. ligustica

        BB/GG

        11

        1

        9.10

        Aegilops tauschii

        DD

        200

        1

        0.50

        Triticum aestivum subsp. aestivum

        BBAuAuDD

        46,225

        80

        0.17

        Triticum aestivum subsp. compactum

        BBAuAuDD

        118

        1

        0.85

        Triticum aestivum subsp. spelta

        BBAuAuDD

        1,292

        6

        0.46

        Triticum hybrid

        BBAADD

        219

        1

        0.46

        Triticum monococcum subsp. aegilopoides

        AmAm

        826

        4

        0.48

        Triticum timopheevii subsp. armeniacum

        GGAuAu

        249

        1

        0.40

        Triticum turgidum subsp. carthlicum

        BBAuAu

        95

        2

        2.11

        Triticum turgidum subsp. dicoccon

        BBAuAu

        622

        10

        1.61

        Triticum turgidum subsp. dicoccoides

        BBAuAu

        777

        2

        0.26

        Triticum turgidum subsp. durum

        BBAuAu

        8,526

        63

        0.74

        Triticum turgidum subsp. paleocolchicum

        BBAuAu

        4

        1

        25

        Triticum turgidum subsp. turanicum

        BBAuAu

        108

        1

        0.93

        Triticum turgidum subsp. turgidum

        BBAuAu

        1,054

        6

        0.57

        Triticum urartu

        AuAu

        245

        3

        1.22

        Triticosecale sp.

        BBAuAuRR

        1,985

        1

        0.05

        Triticum zhukovskyi

        GGAuAuAmAm

        6

        1

        16.67

        Total

         

        62,571

        188

        0.30

        Criteria of selection

        Cancer statistics

        The data used were based on GLOBOCAN 2008 cancer statistics [21]. GLOBOCAN’s cancer statistics are based on the incidence of all cancers using the age-standardized rate (ASR). Our intent was to select wheat lines attributed to specific countries identified in the GLOBOCAN global map (Figure 1) that showed wide variations in cancer incidence rates, under the presumption that these wheat lines, and their close relatives, are likely to be consumed in greater amounts in those countries.
        http://static-content.springer.com/image/art%3A10.1186%2F2048-7010-2-4/MediaObjects/40066_2012_Article_31_Fig1_HTML.jpg
        Figure 1

        A world map of cancer incidence displaying geographic distribution of core collection of wheat germplasm. Estimated age-standardized incidence rate (ASR) per 100,000 residents for all cancers, excluding non-melanoma skin cancer, both sexes and all ages based on GLOBOCAN Cancer statistics, 2008. Each black dot represented a wheat growing country of the world. Four colors ranging from very light yellow to dark brown described the ASR from <103.1 to >326.1 per 100,000 individuals.

        Centers of origin

        Archeological evidence indicates that Armenia, Iran, Iraq, Lebanon, Israel, Jordan, Syria, and Turkey were the centers of origin for wheat germplasm [28]. Cancer statistics also indicated that the occurrence of cancer is very low in these areas, supporting the possibility that the wheat species cultivated and consumed locally provide anticancer protection. Wheat lines from these countries were highly represented in the core collection.

        Regression analysis

        To determine whether the relationship between wheat consumption and cancer incidence was related to geographic origin of wheat, data were collected from the Food and Agriculture Organization of the United Nations (FAOSTAT) from 2007, operationally defined as kg wheat products consumed per capita per year, and from the GLOBOCAN resource from 2008, operationally defined as ASR of cancer incidence at all sites excluding non-melanoma skin cancer. Countries without data for both parameters were excluded from analyses, resulting in a total of 165 countries for the global analysis (Figure 2A) and a subset of the global analysis using 19 Near Eastern countries which are geographically proximate to the origin of wheat (Figure 2B). The countries included in the latter analysis were Armenia, Azerbaijan, Cyprus, Egypt, Georgia, Iran, Israel, Jordan, Kuwait, Lebanon, Pakistan, Saudi Arabia, the Syrian Arab Republic, Tajikistan, Turkey, Turkmenistan, United Arab Emirates, Uzbekistan, and Yemen. No wheat consumption data were available for Iraq through FAOSTAT. Log10-transformed ASRs were regressed on wheat consumption data (10 kg/capita/year) in linear regression analysis using GraphPad Prism vs. 5.02 (GraphPad Software, San Diego, CA, USA). Fit parameters for each analysis, including slope, Y-intercept, R2, and line equations are provided in the figure legend (Figure 2).
        http://static-content.springer.com/image/art%3A10.1186%2F2048-7010-2-4/MediaObjects/40066_2012_Article_31_Fig2_HTML.jpg
        Figure 2

        Linear regression analysis of association between wheat consumption and cancer incidence rates. To determine whether the relationship between wheat consumption and cancer incidence was related to geographic origin of wheat, 2007 wheat consumption data was collected from FAOSTAT, defined as kg wheat products consumed per capita per year, and from the GLOBOCAN resource from 2008, defined as age-standardized rates (ASR) per 100,000 of cancer incidence at all sites excluding non-melanoma skin cancer. ASRs were log10-transformed to satisfy statistical criteria. Countries without data for both parameters were excluded from analyses. (A) All-site cancer incidence ASRs for 165 countries were regressed against yearly wheat consumption, which showed a slightly positive correlation between wheat consumption and cancer incidence. Slope = 0.008940 ± 0.002527; Y-intercept = 2.120 ± 0.02197; R2 = 0.07131; line equation: Log10-transformed ASR = 0.008940*wheat consumption + 2.120. (B) A subset of the global analysis, comprising ASRs for n=19 Near Eastern countries, which are geographically proximate to the origin of wheat, were regressed against wheat consumption data, which showed a slightly negative correlation between wheat consumption and cancer incidence. Slope = −0.006526 ± 0.008315; Y-intercept= 2.187 ± 0.1225; R2 = 0.03497; line equation: Log10-transformed ASR = −0.006526*wheat consumption + 2.187. Analyses were performed using the linear regression analysis function in GraphPad Prism vs. 5.02 (GraphPad Software, San Diego, CA, USA).

        Other considerations

        The species of Triticum and Aegilops include germplasm with three ploidy levels: diploid with genomes Am, B, D, and G; tetraploid with BAu and GAu genomes; and hexaploid with BAuD genomes [28]. Selections within each genome and ploidy level were represented in the core collection.

        Results and discussion

        To our knowledge, there are no published core collections of wheat that have been specifically developed to permit the investigation of wheat for human health benefits and particularly for reducing chronic disease risk using anticancer activity as a screening tool. Thus, the approach used was necessarily descriptive in nature. Rather than enforcing established criteria usually implemented for the development of a core collection for agronomic traits such as disease or pest resistance, or post-harvest processing characteristics [27], cancer incidence data drove variety selection with secondary consideration of ploidy, center of origin, and climate.

        Cancer statistics

        A world map generated from the GLOBOCAN cancer database is shown (Figure 1) and was used to identify the countries from which germplasm was selected from the GRIN domain collection. Based on GLOBOCAN 2008 statistics, the lowest incidence rates of cancer occur in middle Africa, northern Africa, south central Asia, western Africa, eastern Africa, Central America, and western Asia. Interestingly, western Asia, or the Fertile Crescent region between the Tigris and Euphrates river basins, has been determined to be the geographic center of origin for wheat [28]. To explore the relationship between wheat consumption and cancer incidence as it relates to geographic origin of wheat, we used linear regression analysis. When cancer incidence rates for 165 countries were regressed on wheat consumption data in those countries, a slight positive correlation between these parameters was found (Figure 2A, slope = +0.0089 increase in log10-transformed ASR per 10 kg/capita/year increase in wheat consumption). This translates to an increase of 1.02% in cancer incidence for each 10 kg/capita/year increase in wheat consumption. Conversely, when this analysis was confined to 19 countries near the geographic origin of wheat, a slight negative correlation (Figure 2B, slope = −0.0065 increase in log10-transformed ASR per 10 kg/capita/year increase in wheat consumption). This translates to a reduction of 0.99% in cancer incidence for each 10 kg/capita/year increase in wheat consumption. Hence, the slightly positive association between global cancer incidence rates and wheat consumption is reversed when the analysis is restricted only to countries near the geographic origin of wheat (P <0.01). Many other factors are likely involved in the observed correlations between global wheat consumption and cancer incidence rates. Thus, it is important to underscore that there is no evidence of a causal link between these parameters but rather these analyses support the use of cancer incidence by geographic locale as an objective albeit arbitrary tool to guide wheat line selection for the core collection.

        The core collection of wheat germplasm was selected from regions with lower incidence rates of cancer, as well as regions such as North America, Europe, and Oceania (Australia and New Zealand) with higher incidence rates of cancer; evaluation of germplasm from regions of both low and high cancer rates is critical for assessing differences in the type of wheat consumed which may impact cancer activity. In choosing multiple selections from within a country, we were unable to follow the procedure of constant, proportional, and logarithmic selection, as all genotypes were not available in each country [27]. In addition, maintaining uniform diversity around the world was impossible as there are large differences in the total number of accessions in each country that was considered.

        Characterization of selected lines

        A total of 62,571 accessions at GRIN were designated as the source collection, which represented two genera and 14 taxa. From the source collection, 188 accessions were selected for the core collection, which is 0.3% of the source collection. The global distribution of the wheat lines in the core collection is shown (Figure 1, Table 1) and provides a summary of the Triticum and Aegilops species comprising the core collection. The core collection consisted of two genera and 14 taxa of 10 species and was comprised of 19 groups. These 188 accessions belonged to 82 different countries with three different climates (tropical, subtropical, and temperate). The plant introduction number, plant name, taxon, original source, selection criteria, growth habit, and probable market classes are shown (Table 2). Probable market classes were determined by visual observation of the germplasm using a grain color standard and may be changed during future evaluation.
        Table 2

        Detailed information for 188 Triticum and Aegilops germplasm collected from GRIN platform through USDA

        No.

        ID

        Plant name

        Taxon

        Country

        Selection criteria

        Growth habit

        Probable market class

        1

        PI 542274

        84TK081-057

        A. speltoides var. speltoides

        Turkey

        Center of origin

        NA

        NA

        2

        PI 560529

        TU85-008-01

        A. speltoides var. speltoides

        Turkey

        Center of origin

        NA

        NA

        3

        PI 449338

        AE 081D

        A. speltoides var. speltoides

        Israel

        Center of domestication

        NA

        NA

        4

        PI 560528

        TU85-015-02-2

        A. speltoides var. ligustica

        Turkey

        Center of origin

        NA

        NA

        5

        PI 603233

        TA 1669

        A. tauschii

        Azerbaijan

        D genome donor

        NA

        NA

        6

        CItr 180

        China

        T. aestivum subsp. aestivum

        China

        Least breast cancer, highest producer of wheat

        W

        SRW

        7

        CItr 14319

        India Hybrid 65

        T. aestivum subsp. aestivum

        India

        Least breast cancer, second highest producer of wheat

        S

        SWS

        8

        CItr 15136

        American 378

        T. aestivum subsp. aestivum

        Sudan

        Northern Africa

        S

        SWS

        9

        PI 9871

        Erivan

        T. aestivum subsp. aestivum

        Armenia

        Center of origin

        S

        HRS

        10

        PI 9872

        Galgalos

        T. aestivum subsp. aestivum

        Armenia

        Center of origin

        S

        SWS

        11

        PI 52323

        Little Joss

        T. aestivum subsp. aestivum

        UK

        Northern Europe

        W

        SRW

        12

        PI 54431

        Triminia

        T. aestivum subsp. aestivum

        Libya

        Middle East

        S

        HRS

        13

        PI 62004

        NA

        T. aestivum subsp. aestivum

        China

        Least breast cancer

        F

        NA

        14

        PI 81791

        Sapporo Haru Komugi Jugo

        T. aestivum subsp. aestivum

        Japan

        Eastern Asia

        S

        SWS

        15

        PI 82469

        Poubiru

        T. aestivum subsp. aestivum

        North Korea

        Eastern Asia

        S

        HRS

        16

        PI 87117

        Ejuiea

        T. aestivum subsp. aestivum

        South Korea

        Eastern Asia

        W

        HRW

        17

        PI 94418

        99

        T. aestivum subsp. aestivum

        Russia

        Fourth highest producer of wheat

        W

        HRW

        18

        PI 116232

        Solid Straw Tuscan

        T. aestivum subsp. aestivum

        NZ

        High cancer incidence

        W

        SWW

        19

        PI 124818

        Cross No. 7

        T. aestivum subsp. aestivum

        NZ

        High cancer incidence

        S

        HRS

        20

        PI 139599

        Egypt NA 101

        T. aestivum subsp. aestivum

        Egypt

        Western Asia

        S

        SWS

        21

        PI 155315

        Yemen

        T. aestivum subsp. aestivum

        Yemen

        Western Asia

        S

        SRS

        22

        PI 165208

        Sert Bolvadin

        T. aestivum subsp. aestivum

        Turkey

        Center of origin

        S

        SWS

        23

        PI 178383

        6256

        T. aestivum subsp. aestivum

        Turkey

        Center of origin

        W

        SRW

        24

        PI 184994

        Snogg II

        T. aestivum subsp. aestivum

        Norway

        Northern Europe

        S

        HRS

        25

        PI 190451

        Snogg

        T. aestivum subsp. aestivum

        Norway

        Northern Europe

        S

        SRS

        26

        PI 191334

        Marzuolo 87

        T. aestivum subsp. aestivum

        Italy

        Southern Europe

        W

        HWW

        27

        PI 265482

        Olympia

        T. aestivum subsp. aestivum

        Finland

        Northern Europe

        S

        SWS

        28

        PI 266879

        S995

        T. aestivum subsp. aestivum

        Iraq

        Center of origin

        S

        HWS

        29

        PI 266880

        S997

        T. aestivum subsp. aestivum

        Iraq

        Center of origin

        S

        HRS

        30

        PI 274505

        NA

        T. aestivum subsp. aestivum

        Thailand

        South Eastern Asia

        S

        SWS

        31

        PI 283150

        Horani Nawawi

        T. aestivum subsp. aestivum

        Jordan

        Center of origin

        S

        SWS

        32

        PI 297005

        AFRICA MAYO

        T. aestivum subsp. aestivum

        Kenya

        Eastern Africa

        S

        HRS

        33

        PI 347003

        White Shanazi

        T. aestivum subsp. aestivum

        Afghanistan

        South Central Asia

        S

        SWS

        34

        PI 350308

        DACIA

        T. aestivum subsp. aestivum

        Romania

        Eastern Asia

        W

        HRW

        35

        PI 384399

        Nigeria-2

        T. aestivum subsp. aestivum

        Nigeria

        Western Africa

        S

        HWS

        36

        PI 406475

        2

        T. aestivum subsp. aestivum

        Nepal

        South Central Asia

        S

        HRS

        37

        PI 414975

        No. 6

        T. aestivum subsp. aestivum

        Indonesia

        South Central Asia

        S

        HRS

        38

        PI 480034

        MG 31147

        T. aestivum subsp. aestivum

        Ethiopia

        Eastern Africa

        S

        SWS

        39

        PI 487292

        SY 270

        T. aestivum subsp. aestivum

        Jordan

        Center of origin

        S

        HRS

        40

        PI 519554

        PAKISTAN 20

        T. aestivum subsp. aestivum

        Kenya

        Eastern Africa

        S

        SWS

        41

        PI 532053

        96

        T. aestivum subsp. aestivum

        Egypt

        Northern Africa

        S

        SWS

        42

        PI 585019

        15007

        T. aestivum subsp. aestivum

        Saudi Arabia

        Western Asia

        S

        HRS

        43

        PI 585024

        15063

        T. aestivum subsp. aestivum

        Saudi Arabia

        Western Asia (a part of Core 95)

        S

        HRS

        44

        PI 603919

        UCRBW98-2

        T. aestivum subsp. aestivum

        USA

        DNA segment from Spelta and HWS Pavon (bread wheat), Northern America, a part of core 6

        S

        SWS

        45

        PI 648392

        KUNDAN

        T. aestivum subsp. aestivum

        India

        Least breast cancer, second highest producer of wheat

        S

        HWS

        46

        CItr 14352

        II-50-25

        T. aestivum subsp. aestivum

        Paraguay

        South America

        S

        HRS

        47

        PI 10611

        Talimka

        T. aestivum subsp. aestivum

        Turkmenistan

        South Central Asia

        S

        HWS

        48

        PI 61693

        294

        T. aestivum subsp. aestivum

        Malawi

        Eastern Africa

        S

        HWS

        49

        PI 91235

        Cagayan

        T. aestivum subsp. aestivum

        Philippines

        South East Asia

        S

        HRS

        50

        PI 125088

        Ile de France

        T. aestivum subsp. aestivum

        France

        Western Europe, more cancer

        S

        HWS

        51

        PI 174657

        Ile de France

        T. aestivum subsp. aestivum

        France

        Western Europe, more cancer

        S

        SRS

        52

        PI 182665

        9915

        T. aestivum subsp. aestivum

        Lebanon

        Western Asia

        S

        HWS

        53

        PI 191701

        B 256 F.S. 1354

        T. aestivum subsp. aestivum

        Mozambique

        Eastern Africa

        F

        SWS

        54

        PI 191744

        FL S Aurora

        T. aestivum subsp. aestivum

        Mozambique

        Eastern Africa

        S

        SWS

        55

        PI 203081

        Sabanero

        T. aestivum subsp. aestivum

        Tanzania

        Eastern Africa

        S

        HRS

        56

        PI 231115

        II-2734-2c(1–2)x2T

        T. aestivum subsp. aestivum

        Guatemala

        Central America

        S

        HRS

        57

        PI 234233

        Idaho 1877 NR AE

        T. aestivum subsp. aestivum

        Zambia

        Eastern Africa

        S

        HRS

        58

        PI 278386

        Morocco 58

        T. aestivum subsp. aestivum

        Morocco

        Northern Africa

        S

        HRS

        59

        PI 278395

        Poland 2

        T. aestivum subsp. aestivum

        Poland

        Eastern Europe

        W

        HRW

        60

        PI 313098

        Quern

        T. aestivum subsp. aestivum

        Ireland

        Northern Europe

        S

        HRS

        61

        PI 344018

        Mistura Pinto

        T. aestivum subsp. aestivum

        Angola

        Middle Africa, least cancers

        S

        SWS

        62

        PI 344019

        Saraiva Vieira

        T. aestivum subsp. aestivum

        Angola

        Middle Africa, least cancers

        S

        SWS

        63

        PI 351474

        Reval

        T. aestivum subsp. aestivum

        Estonia

        Northern Europe

        W

        HRW

        64

        PI 351870

        10180-54-29

        T. aestivum subsp. aestivum

        Burundi

        Eastern Africa

        S

        SWS

        65

        PI 374248

        BOL-17

        T. aestivum subsp. aestivum

        Chad

        Middle Africa, least cancers

        S

        HRS

        66

        PI 374249

        BOL-19

        T. aestivum subsp. aestivum

        Chad

        Middle Africa, least cancers

        S

        HRS

        67

        PI 374254

        34335

        T. aestivum subsp. aestivum

        Mali

        Western Africa

        S

        HWS

        68

        PI 384399

        Nigeria-2

        T. aestivum subsp. aestivum

        Nigeria

        Western Africa

        S

        HWS

        69

        PI 410425

        ILICHEVKA

        T. aestivum subsp. aestivum

        Kazakhstan

        South Central Asia

        W

        SRW

        70

        PI 428690

        LEUCURUM 3

        T. aestivum subsp. aestivum

        Uzbekistan

        South Central Asia

        S

        SRS

        71

        PI 470905

        MG 18060

        T. aestivum subsp. aestivum

        Algeria

        Northern Africa

        S

        SWS

        72

        PI 480481

        R-124

        T. aestivum subsp. aestivum

        Bolivia

        South America

        S

        SRS

        73

        PI 481713

        41

        T. aestivum subsp. aestivum

        Bhutan

        South Central Asia

        W

        HRW

        74

        PI 481715

        Ka

        T. aestivum subsp. aestivum

        Bhutan

        South Central Asia

        S

        SWS

        75

        PI 486155

        CHIWORE

        T. aestivum subsp. aestivum

        Zimbabwe

        Eastern Africa, least breast cancer

        S

        HRS

        76

        PI 486156

        GWEBI

        T. aestivum subsp. aestivum

        Zimbabwe

        Eastern Africa, least breast cancer

        S

        SWS

        77

        PI 486157

        RUSAPE

        T. aestivum subsp. aestivum

        Zimbabwe

        Eastern Africa, least breast cancer

        S

        HRS

        78

        PI 490405

        Koira alkuna

        T. aestivum subsp. aestivum

        Mali

        Western Africa

        S

        HWS

        79

        PI 494926

        ZFA 3145

        T. aestivum subsp. aestivum

        Zambia

        Eastern Africa

        S

        HRS

        80

        PI 532301

        Alas

        T. aestivum subsp. aestivum

        Oman

        Western Asia

        S

        SRS

        81

        PI 573754

        NSGC 531

        T. aestivum subsp. aestivum

        Hondurus

        Central America

        S

        HRS

        82

        PI 591964

        EMBRAPA 16

        T. aestivum subsp. aestivum

        Brazil

        South America

        S

        HRS

        83

        PI 639354

        TJK03-128

        T. aestivum subsp. aestivum

        Tazikistan

        South Central Asia

        S

        SWS

        84

        PI 648894

        Dickson's No. 444

        T. aestivum subsp. aestivum

        Argentina

        South America

        S

        HWS

        85

        Cltr 14108

        Chinese Spring

        T. aestivum subsp. aestivum

        USA

        Northern America

        S

        SRS

        86

        PI 434642

        TINCURRIN

        T. aestivum subsp. compactum

        Australia

        More cancer especially skin cancer

        S

        Club wheat

        87

        PI 190963

        Spelta Hohenheim

        T. aestivum subsp. spelta

        Portugal

        Southern Europe

        S

        Spelt

        88

        PI 348710

        69Z6.894

        T. aestivum subsp. spelta

        Spain

        Southern Europe

        S

        Spelt

        89

        PI 355625

        Spelta 34

        T. aestivum subsp. spelta

        Belgium

        Western Europe

        S

        Spelt

        90

        PI 591895

        NA

        T. aestivum subsp. spelta

        Germany

        Central Europe

        W

        Spelt

        91

        PI 367199

        128

        T. aestivum subsp. spelta

        Afghanistan

        Central Asia

        W

        Spelt

        92

        PI 538510

        G2830

        T. monococcum subsp. aegilopoides

        Iraq

        Center of origin, Western Asia

        S

        Wild einkorn

        93

        PI 167526

        2485

        T. monococcum subsp. aegilopoides

        Turkey

        Western Asia

        S

        Wild einkorn

        94

        PI 266844

        87

        T. monococcum subsp. aegilopoides

        Uk

        Northern Europe

        S

        Wild einkorn

        95

        PI 427990

        G3114

        T. monococcum subsp. aegilopoides

        Lebanon

        Center of domestication

        W

        Wild einkorn

        96

        PI 427304

        G1764

        T. timopheevii subsp. armeniacum

        Armenia

        Center of origin, Western Asia

        W

        Wild timopheevii

        97

        PI 538478

        G2633

        T. timopheevii subsp. armeniacum

        Iraq

        Center of domestication

        W

        Wild timopheevii

        98

        PI 70738

        22

        T. turgidum subsp. carthlicum

        Iraq

        Center of origin, Western Asia

        S

        Persian wheat

        99

        PI 532501

        H83-1537

        T. turgidum subsp. carthlicum

        Soviet Union

         

        S

        Persian wheat

        100

        PI 471808

        G-485-5 M

        T. turgidum subsp. dicoccoides

        Israel

        Center of domestication

        W

        Wild emmer

        101

        PI 471778

        G-40-1-2B-1 M

        T. turgidum subsp. dicoccoides

        Israel

        Center of domestication

        W

        Wild emmer

        102

        PI 2789

        Yaroslav Spring

        T. turgidum subsp. dicoccon

        Russia

        Fourth highest producer of wheat

        S

        Cultivated emmer

        103

        PI 73388

        2868

        T. turgidum subsp. dicoccon

        Armenia

        Center of origin, Western Asia

        S

        Cultivated emmer

        104

        PI 79899

        N-64

        T. turgidum subsp. dicoccon

        China

        Least breast cancer, highest producer of wheat

        S

        Cultivated emmer

        105

        PI 190920

        2323A

        T. turgidum subsp. dicoccon

        Portugal

        Southern Europe

        S

        Cultivated emmer

        106

        PI 191390

        Rufum

        T. turgidum subsp. dicoccon

        Ethiopia

        Eastern Africa

        S

        Cultivated emmer

        107

        PI 308879

        NA

        T. turgidum subsp. dicoccon

        Spain

        Southern Europe

        S

        Cultivated emmer

        108

        PI 355483

        T 563

        T. turgidum subsp. dicoccon

        Spain

        Southern Europe

        S

        Cultivated emmer

        109

        PI 355485

        T 567

        T. turgidum subsp. dicoccon

        Spain

        Southern Europe

        S

        Cultivated emmer

        110

        PI 499973

        KU 1533

        T. turgidum subsp. dicoccon

        Armenia

        Center of origin, Western Asia

        S

        Cultivated emmer

        111

        PI 154582

        NA

        T. turgidum subsp. dicoccon

        Taiwan

        Eastern Asia

        S

        Cultivated emmer

        112

        CItr 15185

        Hudeiba 154

        T. turgidum subsp. durum

        Sudan

        Northern Africa

        S

        Durum or macaroni

        113

        PI 9130

        Saragolla

        T. turgidum subsp. durum

        Italy

        Southern Europe

        S

        Durum or macaroni

        114

        PI 54432

        Tripshiro

        T. turgidum subsp. durum

        Libya

        Northern Africa

        S

        Durum or macaroni

        115

        PI 67341

        Huguenot

        T. turgidum subsp. durum

        Australia

        More cancer especially skin cancer

        S

        Durum or macaroni

        116

        PI 78809

        CI 10107

        T. turgidum subsp. durum

        Georgia

        Western Asia

        S

        Durum or macaroni

        117

        PI 81792

        Marching No. 8

        T. turgidum subsp. durum

        Japan

        Eastern Asia

        S

        Durum or macaroni

        118

        PI 94701

        390

        T. turgidum subsp. durum

        Ancient Palestine

        Western Asia

        S

        Durum or macaroni

        119

        PI 133459

        Durum H2

        T. turgidum subsp. durum

        Egypt

        Center of origin, Northern Africa

        S

        Durum or macaroni

        120

        PI 153726

        Sicilian

        T. turgidum subsp. durum

        N. Africa

        Less cancers

        S

        Durum or macaroni

        121

        PI 157955

        Francesone

        T. turgidum subsp. durum

        Italy

        Southern Europe

        S

        Durum or macaroni

        122

        PI 174645

        Huguenot

        T. turgidum subsp. durum

        Australia

        More cancer especially skin cancer

        S

        Durum or macaroni

        123

        PI 182113

        S-44

        T. turgidum subsp. durum

        Pakistan

        South Central Asia

        S

        Durum or macaroni

        124

        PI 184532

        Russia

        T. turgidum subsp. durum

        Russia

        Europe

        S

        Durum or macaroni

        125

        PI 208908

        Mendola

        T. turgidum subsp. durum

        Iraq

        Center of origin

        S

        Durum or macaroni

        126

        PI 208910

        Sin El-Jamil

        T. turgidum subsp. durum

        Iraq

        Center of origin

        S

        Durum or macaroni

        127

        PI 210848

        7979

        T. turgidum subsp. durum

        Iran

        South Central Asia

        S

        Durum or macaroni

        128

        PI 221702

        11

        T. turgidum subsp. durum

        Indonesia

        Southern Eastern Asia

        S

        Durum or macaroni

        129

        PI 231380

        Saragolla

        T. turgidum subsp. durum

        Italy

        Oldest durum variety in Italy

        S

        Durum or macaroni

        130

        PI 261823

        Namra

        T. turgidum subsp. durum

        Saudi Arabia

        Western Asia

        S

        Durum or macaroni

        131

        PI 265017

        796

        T. turgidum subsp. durum

        Serbia

        Southern Europe

        S

        Durum or macaroni

        132

        PI 278223

        Gartons Early Cone

        T. turgidum subsp. durum

        UK

        Northern Europe

        W

        Durum or macaroni

        133

        PI 278258

        Greece 1

        T. turgidum subsp. durum

        Greece

        Southern Europe

        S

        Durum or macaroni

        134

        PI 278509

        Valencia 6

        T. turgidum subsp. durum

        Spain

        Southern Europe

        S

        Durum or macaroni

        135

        PI 278553

        Tripolitco

        T. turgidum subsp. durum

        Cyprus

        Western Asia

        S

        Durum or macaroni

        136

        PI 283853

        China 34

        T. turgidum subsp. durum

        China

        Least breast cancer, highest producer of wheat

        S

        Durum or macaroni

        137

        PI 306571

        R.S.N.

        T. turgidum subsp. durum

        Italy

        Southern Europe

        S

        Durum or macaroni

        138

        PI 325850

        PW 3

        T. turgidum subsp. durum

        India

        Least breast cancer, second highest producer of wheat

        S

        Durum or macaroni

        139

        PI 361149

        Bijaga Yellow

        T. turgidum subsp. durum

        India

        Least breast cancer, second highest producer of wheat

        S

        Durum or macaroni

        140

        PI 362046

        C 1138/63

        T. turgidum subsp. durum

        Romania

        Eastern Europe

        W

        Durum or macaroni

        141

        PI 422295

        QUILAFEN

        T. turgidum subsp. durum

        Chile

        South America

        S

        Durum or macaroni

        142

        PI 422297

        SINCAPE 90

        T. turgidum subsp. durum

        Italy

        Southern Europe

        S

        Durum or macaroni

        143

        PI 422312

        MACS-45

        T. turgidum subsp. durum

        India

        Least breast cancer, second highest producer of wheat

        S

        Durum or macaroni

        144

        PI 428458

        Egypt Local No. 8

        T. turgidum subsp. durum

        Egypt

        Center of origin, Northern Africa

        S

        Durum or macaroni

        145

        PI 428468

        JORDAN 38

        T. turgidum subsp. durum

        Jordan

        Center of origin, Western Asia

        S

        Durum or macaroni

        146

        PI 428469

        JORDAN 40

        T. turgidum subsp. durum

        Jordan

        Center of origin, Western Asia

        S

        Durum or macaroni

        147

        PI 462107

        172

        T. turgidum subsp. durum

        Yemen

        Western Asia

        S

        Durum or macaroni

        148

        PI 480347

        MG 31577

        T. turgidum subsp. durum

        Ethiopia

        Eastern Africa

        S

        Durum or macaroni

        149

        PI 496260

        MEDORA

        T. turgidum subsp. durum

        Canada

        North America

        S

        Durum or macaroni

        150

        PI 519864

        DURUM VARIETY 24

        T. turgidum subsp. durum

        Mexico

        North America

        S

        Durum or macaroni

        151

        PI 520393

        TUNISIAN DURUM 1

        T. turgidum subsp. durum

        Tunisia

        Northern Africa

        S

        Durum or macaroni

        152

        PI 520394

        TUNISIAN DURUM 8

        T. turgidum subsp. durum

        Tunisia

        Northern Africa

        S

        Durum or macaroni

        153

        PI 520414

        ICD 7780-5AP-OSH-OAP

        T. turgidum subsp. durum

        Syria

        Center of origin, Western Asia

        S

        Durum or macaroni

        154

        PI 520415

        SYRIAN DURUM 27

        T. turgidum subsp. durum

        Syria

        Center of origin, Western Asia

        S

        Durum or macaroni

        155

        PI 542464

        SHORT SARAGOLLA

        T. turgidum subsp. durum

        USA

        High cancer incidence

        S

        Durum or macaroni

        156

        PI 585025

        15017

        T. turgidum subsp. durum

        Saudi Arabia

        Western Asia

        S

        Durum or macaroni

        157

        CItr 14374

        497-360

        T. turgidum subsp. durum

        Lebanon

        Western Asia

        S

        Durum or macaroni

        158

        CItr 14802

        ELS 6404-122

        T. turgidum subsp. durum

        Eritrea

        Eastern Africa

        S

        Durum or macaroni

        159

        PI 5465

        Candeal

        T. turgidum subsp. durum

        Argentina

        South America

        F

        Durum or macaroni

        160

        PI 5639

        Kubanka

        T. turgidum subsp. durum

        Kazakhstan

        South Central Asia, largest consumer of wheat

        S

        Durum or macaroni

        161

        PI 35314

        1809a

        T. turgidum subsp. durum

        Kyrgyzstan

        South Central Asia

        F

        Durum or macaroni

        162

        PI 50929

        933

        T. turgidum subsp. durum

        Kyrgyzstan

        South Central Asia

        S

        Durum or macaroni

        163

        PI 61108

        6951

        T. turgidum subsp. durum

        Turkmenistan

        South Central Asia

        S

        Durum or macaroni

        164

        PI 89642

        NA

        T. turgidum subsp. durum

        Hondurus

        Central America

        S

        Durum or macaroni

        165

        PI 278384

        Morocco C10895

        T. turgidum subsp. durum

        Morocco

        Northern Africa

        W

        Durum or macaroni

        166

        PI 286066

        NA

        T. turgidum subsp. durum

        Poland

        Eastern Europe

        S

        Durum or macaroni

        167

        PI 384401

        Wurno 2

        T. turgidum subsp. durum

        Nigeria

        Western Africa

        S

        Durum or macaroni

        168

        PI 519759

        D 73121

        T. turgidum subsp. durum

        Algeria

        Northern Africa

        S

        Durum or macaroni

        169

        PI 520164

        ALGERIA LINE 47

        T. turgidum subsp. durum

        Algeria

        Northern Africa

        S

        Durum or macaroni

        170

        PI 532289

        Musane

        T. turgidum subsp. durum

        Oman

        Western Asia

        S

        Durum or macaroni

        171

        PI 565208

        Chaggo

        T. turgidum subsp. durum

        Bolivia

        South America

        S

        Durum or macaroni

        172

        PI 592019

        VATAN

        T. turgidum subsp. durum

        Uzbekistan

        South Central Asia

        S

        Durum or macaroni

        173

        PI 654290

        TJK2006:296

        T. turgidum subsp. durum

        Tazikistan

        South Central Asia

        S

        Durum or macaroni

        174

        Cltr 13165

        Langdon

        T. turgidum subsp. durum

        USA

        Northern America

        W

        Durum or macaroni

        175

        PI 330553

        189

        T. turgidum subsp. paleocolchicum

        UK

        Northern Europe

        S

        Cultivated emmer

        176

        PI 211708

        Egypt

        T. turgidum subsp. turanicum

        Egypt

        Center of origin, Northern Africa

        S

        Khorasan or oriental

        177

        PI 166591

        Ak

        T. turgidum subsp. turgidum

        Turkey

        Center of origin

        S

        Rivet or cone

        178

        PI 167867

        4314

        T. turgidum subsp. turgidum

        Turkey

        Center of origin

        S

        Rivet or cone

        179

        PI 481591

        IQ 223

        T. turgidum subsp. turgidum

        Iraq

        Center of origin

        S

        Rivet or cone

        180

        PI 502933

        Fo Shou Mai

        T. turgidum subsp. turgidum

        China

        Largest producer

        S

        Rivet or cone

        181

        PI 208912

        Zerdakia

        T. turgidum subsp. turgidum

        Iraq

        Center of origin

        S

        Rivet or cone

        182

        PI 438971

        AKMOLINKA 2

        T. turgidum subsp. turgidum

        Kazakhstan

        South Central Asia

        S

        Rivet or cone

        183

        PI 427328

        G2264

        T. urartu

        Iraq

        Center of origin

        S

        Wild einkorn

        184

        PI 428183

        G1759

        T. urartu

        Armenia

        Center of origin

        S

        Wild einkorn

        185

        PI 428279

        G3162

        T. urartu

        Lebanon

        Center of domestication

        W

        Wild einkorn

        186

        PI 355707

        69Z5.72

        T. zhukovskyi

        Georgia

        Donor for GG genome and cross between T. timopheevi and T. monococcum

        W

        Cultivated hexaploid

        187

        PI 429099

        6A-696

        Triticosecale sp.

        Germany

        Cross between T. dicoccum & S. cereale; hexaploid

        F

        Tritical (Rye and durum cross)

        188

        PI 574284

        ASVM4*4654

        T. hybrid

        USA

        High cancer incidence

        S

        Aegilops squarrosa/T. dicoccum

        A, Aegilops; F, Facultative; HRW, Hard red winter; HRS, Hard red spring; HWS, Hard white spring; HWW, Hard white winter; NA, not available; S, Spring; W, Winter; SRS, Soft red spring; SRW, Soft red winter; SWS, Soft white spring; SWW, Soft white winter; T, Triticum.

        Climate

        There are several climates in which the domestication of wheat occurred: tropical, subtropical, and temperate, and three types of wheat resulted: winter, spring, and facultative. They differ in temperature response due to the presence and absence of dominant vernalization genes [29, 30]. The three types of wheat are presented in the core collection.

        Limitations

        Cancer prevalence rates among countries are subject to a host of genetic and environmental determinants. Despite associations reported between wheat consumption and cancer risk, there is no direct causal evidence that a particular wheat variety reduces the cancer rate within a specific country [19]. Nonetheless, the overall cancer rate in a country provided an objective albeit arbitrary criterion for selecting wheat lines for inclusion in the core collection. The usefulness of this approach will be determined as screening for anticancer activity in laboratory model systems progresses. Another limitation is that many core collections of crop species are between 5% and 10% of the domain in size, and thus the core collection reported is relatively small in comparison (Table 1). However, there are examples of core collections <5% of the domain in size. For example, the international barley core collection is approximately 0.3% of the world barley holding, and the ICRISAT (International Crops Research Institute for the Semi Arid Crops, Hyderabad, India) sorghum core collection is about 1.5% of the domain size [31, 32]. As many of the lines shown (Table 2) are wild accessions, data are not available on genetic and metabolic markers, agronomic and morphological characteristics, thus limiting the descriptive information provided.

        Future direction

        Having established this core collection and obtained grain for each line from GRIN, the next step in the identification of distinct wheat lines with enhanced biomedical activity is the interrogation of these lines via phytochemical profiles using LC-TOF-MS analysis of wheat grain extracts according to our recently published procedures [9]. The chromatographic data that result will be subjected to advanced multivariate regression techniques that plot multidimensional relationships to define the chemical diversity within the core collection. The same extracts used for metabolic profiling will then be subjected to in-vitro biological analysis to assign a relative value for anticancer activity to each wheat line. For wheat lines with the greatest in-vitro activity, in-vivo testing in appropriate animal cancer models will be conducted. For wheat lines with in-vivo anticancer activity, the genetic and metabolomic traits that account for protection will be identified and appropriate experiments conducted to determine the extent to which environmental factors impact the stable expression of the traits of interest [10].

        Conclusion

        While there has been an active discussion of adding value to wheat through the enhancement of its human health benefits, no systematic approaches have been establish to advance this effort. The work reported herein constitutes the first essential step needed to examine wheat germplasm resources in order to identify health benefits that may exist and to develop them fully for the benefit of the consuming public.

        Availability of supporting data

        The datasets supporting the results of this article are available in the Germplasm Resources Information Network (GRIN) repository from the United States Department of Agriculture (USDA), http://​www.​ars-grin.​gov/​npgs/​index.​html; in the Food and Agriculture Organization of the United States (FAOSTAT) repository from the World Health Organization, http://​faostat3.​fao.​org/​home/​index.​html#COMPARE; and in the GLOBOCAN repository from the International Agency for Research on Cancer (IARC), http://​globocan.​iarc.​fr.

        Authors’ information

        MS is a Research Associate in the Department of Soil and Crop Sciences, SM is a doctoral candidate in the Cell and Molecular Biology Program, and HT directs the Cancer Prevention Laboratory at Colorado State University.

        Abbreviations

        ASR: 

        Age-standardized rate per 100,000 individuals

        CC: 

        Core collection

        GRIN: 

        Germplasm Resources Information Network

        mt: 

        Metric tons

        PI: 

        Plant introduction.

        Declarations

        Acknowledgments

        The authors would like to thank Dr. Harold Bockelman for providing wheat germplasm from GRIN, the International Agency for Research on Cancer for allowing us to use the GLOBOCAN cancer map, and Stephanie MacLeaod and John McGinley for their assistance in the preparation of this manuscript. The authors would also like to thank Colorado State University Libraries Open Access Research and Scholarship program for providing funds for publication.

        Authors’ Affiliations

        (1)
        Cancer Prevention Laboratory, Colorado State University 1173 Campus Delivery

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