Email updates

Keep up to date with the latest news and content from Agriculture & Food Security and BioMed Central.

Open Access Research

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

Meenakshi Santra, Shawna B Matthews and Henry J Thompson*

Author Affiliations

Cancer Prevention Laboratory, Colorado State University, 1173 Campus Delivery, Fort Collins, CO, 80523, USA

For all author emails, please log on.

Agriculture & Food Security 2013, 2:4  doi:10.1186/2048-7010-2-4


The electronic version of this article is the complete one and can be found online at: http://www.agricultureandfoodsecurity.com/content/2/1/4


Received:26 September 2012
Accepted:29 January 2013
Published:15 February 2013

© 2013 Santra et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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 [1-8]. 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 [14-16], and, most importantly, are also considered preventable through lifestyle choices of which diet is considered to play a prominent role [17-19].

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 theTriticumandAegilopsspecies used for core collection

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.

thumbnailFigure 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).

thumbnailFigure 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 188TriticumandAegilopsgermplasm collected from GRIN platform through USDA

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 webcite; 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 webcite; and in the GLOBOCAN repository from the International Agency for Research on Cancer (IARC), http://globocan.iarc.fr webcite.

Abbreviations

ASR: Age-standardized rate per 100,000 individuals; CC: Core collection; GRIN: Germplasm Resources Information Network; mt: Metric tons; PI: Plant introduction.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

MS directed the selection of specific species from GRIN, SM participated in data analysis and germplasm selection, and HT provided overall direction and specific guidance relative to interpretation of the cancer prevalence data. All authors participated in writing the manuscript. All authors read and approved the final manuscript.

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.

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.

References

  1. Arthur AE, Peterson KE, Rozek LS, Taylor JM, Light E, Chepeha DB, Hebert JR, Terrell JE, Wolf GT, Duffy SA: Pretreatment dietary patterns, weight status, and head and neck squamous cell carcinoma prognosis.

    Am J Clin Nutr 2013, 97:360-368. PubMed Abstract | Publisher Full Text OpenURL

  2. Cohen LA, Zhao Z, Zang EA, Wynn TT, Simi B, Rivenson A: Wheat bran and psyllium diets: effects on N-methylnitrosourea-induced mammary tumorigenesis in F344 rats.

    J Natl Cancer Inst 1996, 88:899-907. PubMed Abstract | Publisher Full Text OpenURL

  3. Fung TT, Hu FB, Pereira MA, Liu S, Stampfer MJ, Colditz GA, Willett WC: Whole-grain intake and the risk of type 2 diabetes: a prospective study in men.

    Am J Clin Nutr 2002, 76:535-540. PubMed Abstract | Publisher Full Text OpenURL

  4. Gil A, Ortega RM, Maldonado J: Wholegrain cereals and bread: a duet of the Mediterranean diet for the prevention of chronic diseases.

    Public Health Nutr 2011, 14:2316-2322. PubMed Abstract | Publisher Full Text OpenURL

  5. Jacobs DR, Marquart LF, Slavin J: Whole grain intake and cancer: an expanded review and meta analysis.

    FASEB J 1998, 12:A875. OpenURL

  6. Pereira MA, Jacobs DR Jr, Pins JJ, Raatz SK, Gross MD, Slavin JL, Seaquist ER: Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults.

    Am J Clin Nutr 2002, 75:848-855. PubMed Abstract | Publisher Full Text OpenURL

  7. Schatzkin A, Mouw T, Park Y, Subar AF, Kipnis V, Hollenbeck A, Leitzmann MF, Thompson FE: Dietary fiber and whole-grain consumption in relation to colorectal cancer in the NIH-AARP Diet and Health Study.

    Am J Clin Nutr 2007, 85:1353-1360. PubMed Abstract | Publisher Full Text OpenURL

  8. Tabung F, Steck SE, Su LJ, Mohler JL, Fontham ET, Bensen JT, Hebert JR, Zhang H, Arab L: Intake of grains and dietary fiber and prostate cancer aggressiveness by race.

    Prostate Cancer 2012, 201:323296. OpenURL

  9. Matthews SB, Santra M, Mensack MM, Wolfe P, Byrne PF, Thompson HJ: Metabolite profiling of a diverse collection of wheat lines using ultraperformance liquid chromatography coupled with time-of-flight mass spectrometry.

    PLoS One 2012, 7:e44179. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  10. Thompson MD, Thompson HJ: Biomedical agriculture: a systematic approach to food crop improvement for chronic disease prevention.

    Adv Agron 2009, 102:1-54. OpenURL

  11. Thompson HJ: Vegetable and fruit intake and the development of cancer: a brief review and analysis. In Bioactive Foods in Promoting Health. Edited by Watson RR, Preedy VR. Oxford: Academic; 2010:19-36. OpenURL

  12. Centers for Disease Control: Health, United States, 2007. Atlanta, GA: Centers for Disease Control; 2007. OpenURL

  13. World Health Organization: Chronic Disease. Geneva: WHO; 2008. OpenURL

  14. Marshall S: Role of insulin, adipocyte hormones, and nutrient-sensing pathways in regulating fuel metabolism and energy homeostasis: a nutritional perspective of diabetes, obesity, and cancer.

    Sci STKE 2006, 2006:re7. PubMed Abstract | Publisher Full Text OpenURL

  15. Hirsch HA, Iliopoulos D, Joshi A, Zhang Y, Jaeger SA, Bulyk M, Tsichlis PN, Shirley Liu X, Struhl K: A transcriptional signature and common gene networks link cancer with lipid metabolism and diverse human diseases.

    Cancer Cell 2010, 17:348-361. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  16. Tacutu R, Budovsky , Yanai H, Fraifeld VE: Molecular links between cellular senescence, longevity and age-related diseases - a systems biology perspective.

    Aging 2011, 3:1178-1191. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  17. Ezzati M, Riboli E: Can noncommunicable diseases be prevented? Lessons from studies of populations and individuals.

    Science 2012, 337:1482-1487. PubMed Abstract | Publisher Full Text OpenURL

  18. Eyre H, Kahn R, Robertson RM, Clark NG, Doyle C, Hong Y, Gansler T, Glynn T, Smith RA, Taubert K, Thun MJ: Preventing cancer, cardiovascular disease, and diabetes: a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association.

    Circulation 2004, 109:3244-3255. PubMed Abstract | Publisher Full Text OpenURL

  19. WCRF/AICR: Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. Washington, DC: AICR; 2007. OpenURL

  20. Spring B, Moller AC, Coons MJ: Multiple health behaviours: overview and implications.

    J Public Health (Oxf) 2012, Suppl 1:i3-i10. OpenURL

  21. International Agency for Research on Cancer: [http://globocan.iarc.fr/factsheets/cancers/all.asp] webcite

    Cancer Incidence, Mortality and Prevalence Worldwide in 2008. Lyon: IARC; 2008. OpenURL

  22. FAOSTAT: [http://faostat.org] webcite

    Production of the world's most important grain crops. 2008. PubMed Abstract | Publisher Full Text OpenURL

  23. Carver BF: Wheat Science and Trade. Ames, IA: Wiley-Blackwell; 2009. OpenURL

  24. Gooding MJ, Davies WP: Wheat Production and Utilization. London: CAB International; 1997. OpenURL

  25. Stallknecht GF, Gilbertson KM, Ranney JE: Alternative wheat cereals as food grains: Einkorn, emmer, spelt, kamut, and triticale. In Progress in new crops. Edited by Janick J. Alexandria, VA: ASHS Press; 1996:156-170. OpenURL

  26. National Plant Germplasm System[http://www.ars-grin.gov/cgi-bin/npgs] webcite

    2012.

  27. Brown AHD: Core collections: a practical approach to genetic resources management.

    Genome 1989, 31:818-824. Publisher Full Text OpenURL

  28. Hancock JF: Plant evolution and the origin of crop species. Wallingford: CABI Pub; 2004. OpenURL

  29. Sun QM, Zhou RH, Gao LF, Zhao GY, Jia JZ: The characterization and geographical distribution of the genes responsible for vernalization requirement in Chinese bread wheat.

    J Integr Plant Biol 2009, 51:423-432. PubMed Abstract | Publisher Full Text OpenURL

  30. Preston JC, Kellogg EA: Discrete developmental roles for temperate cereal grass VERNALIZATION1/FRUITFULL-like genes in flowering competency and the transition to flowering.

    Plant Physiol 2008, 146:265-276. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  31. Van Hintum TJL: Core collections of plant genetic resources. In PGRI Technical Bulletin No.3. Edited by Brown AHD, Spillane C, Hodgkin T. Rome: International Plant Genetic Resources Institute; 2000:6-51. OpenURL

  32. van Hintum TJL: The Core Selector, a system to generate representative selections of germplasm accessions.

    Plant Genet Resour Newsl 1999, 118:64-67. OpenURL